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J Dent Res 85(7):658-663, 2006
© 2006 International and American Associations for Dental Research

RESEARCH REPORT
Biological

Increase of Galanin in Trigeminal Ganglion during Tooth Movement

T. Deguchi1, T. Yabuuchi1, R. Ando1, H. Ichikawa3, T. Sugimoto3, and T. Takano-Yamamoto1,2,*

1 Department of Orthodontics and Dentofacial Orthopedics, Okayama University Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, 2-5-1, Shikata-cho, Okayama, 700-8525, Japan;
2 Research Center for Biomedical Engineering, Okayama University, 2-5-1, Shikata-cho, Okayama, 700-8525, Japan; and
3 Department of Oral Function and Anatomy, and Biodental Research Center, Okayama University Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, 2-5-1, Shikata-cho, Okayama, 700-8525, Japan

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


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
It is known that nerve fibers containing neuropeptides such as galanin increase in the periodontal ligament during experimental tooth movement. However, the origin of galanin-containing nerve fibers in the periodontal ligament remains unclear. This study was conducted to examine our hypothesis that the increased galanin nerve fibers have a sensory neuronal origin, and that the peptide is associated with pain transmission and/or periodontal ligament remodeling during experimental tooth movement. In control rats, galanin-immunoreactive trigeminal ganglion cells were very rare and were observed predominantly in small ganglion cells. After 3 days of experimental tooth movement, galanin-immunoreactive trigeminal ganglion cells significantly increased, and the most marked increase was observed at 5 days after experimental tooth movement. Furthermore, their cell size spectrum also significantly changed after 3 and 5 days of movement: Medium-sized and large trigeminal ganglion cells began expressing, and continued to express, galanin until 14 days after experimental tooth movement. These findings suggest that the increase of galanin in the periodontal ligament during experimental tooth movement at least partially originates from trigeminal ganglion neurons and may play a role in pain transmission and/or periodontal remodeling.

KEY WORDS: galanin • tooth movement • trigeminal ganglion • rat


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The periodontal ligament is partly innervated by primary sensory neurons in the trigeminal ganglion (Byers, 1985; Byers and Dong, 1989). These neurons are of various cell body sizes in the ganglion. Trigeminal ganglion neurons are considered to transmit nociceptive and mechanoreceptive information from the periodontal ligament to the brainstem (Byers, 1985). Experimental tooth movement causes several changes in periodontal tissues such as the blood vessels, bone, and periodontal ligament (Takano-Yamamoto et al., 1992). In the periodontal ligament, nerve fibers also increase in number during orthodontic tooth movement; numerous free nerve endings and perivascular endings appear in the apical region of the periodontal ligament (Kvinnsland and Kvinnsland, 1990; Saito et al., 1991). These nerve fibers are considered to be associated with the pain and discomfort that patients experience during orthodontic tooth movement (Brown and Moerenhout, 1991). It is also possible that periodontal nerve fibers play a role in remodeling of the periodontal tissues during orthodontic tooth movement.

Recently, we demonstrated an increase in the number of galanin-containing nerve fibers in the periodontal ligament (Deguchi et al., 2003). A few galanin-containing nerve fibers have been observed in the normal rat periodontal ligament. In the normal trigeminal ganglion, galanin is localized to small neurons that are probably nociceptors in the oro-facial regions (Ch’ng et al., 1985; Skofitsch and Jacobowitz, 1985; Ju et al., 1987). However, little is known about the origin of galanin in the periodontal ligament during experimental tooth movement.

The normal periodontal ligament contains calcitonin gene-related peptide (CGRP) (Silverman and Kruger, 1987). This peptide has been detected in free nerve endings and perivascular endings, and experimental tooth movement increased the number of these CGRP-containing nerve fibers (Kvinnsland and Kvinnsland, 1990; Saito et al., 1991). It is considered that periodontal CGRP is involved in pain transmission, inflammatory response, and/or periodontal ligament remodeling. In the normal trigeminal ganglion, CGRP is mostly located in small to medium-sized neurons (Skofitsch and Jacobowitz, 1985). Small CGRP-containing neurons co-express galanin, whereas medium-sized CGRP-containing neurons do not. However, there has not been any report investigating changes in the distribution of neuropeptides or the relationship between CGRP and galanin in the trigeminal ganglion during experimental tooth movement.

We hypothesized that experimental tooth movement increases galanin expression in trigeminal neurons, and that the increased peptide has an effect on remodeling of the PDL and/or pain transmission. In addition, galanin and CGRP may function co-operatively during tooth movement. Thus, in the present study, we investigated the distribution of neurons with galanin immunoreactivity and its co-expression with CGRP immunoreactivity in the trigeminal ganglion during experimental tooth movement in rats.


   MATERIALS & METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Experimental Tooth Movement and Tissue Preparation
In total, 42 adult male Sprague-Dawley rats (body weight, from 200 to 250 g each) were used in this study. Thirty-six rats were deeply anesthetized with pentobarbital sodium (40 mg/kg, i.p.), and a piece of elastic band (1 x 1 x 0.8 mm) was then inserted interproximally between the mandibular right first and second molars (Fig. 1Go). After 1, 3, 5, 7, 14, and 28 days, rats were re-anesthetized with ether until respiration was suppressed, then transvascularly perfused with 50 mL of saline, followed by 500 mL of 4% formaldehyde in 0.1 M phosphate buffer (pH 7.4). The remaining 6 rats that did not have the elastic placed were used as the control group. Right trigeminal ganglia were dissected, soaked overnight in 20% sucrose in phosphate buffer, and then cut horizontally into 10-µm-thick serial sections, with the use of a cryostat.


Figure 1
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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 mandibular first (M1) and second (M2) molars.

 
Immunohistochemistry
For galanin immunohistochemistry, the ABC (avidin-biotin-horseradish peroxidase complex) method was performed. Sections were incubated with rabbit anti-galanin serum (1:80,000; Peninsula Laboratories Inc., Belmont, CA, USA) or rabbit anti-CGRP (1:50,000; Peninsula Laboratories Inc.) for 3 days at 4°C, followed by sequential incubation with biotinylated anti-rabbit IgG (Vector Labs., Burlingame, CA, USA) for 1 hr and with ABC complex for 1 hr at room temperature. Immunoreactive products were visualized by the nickel ammonium sulfate-intensified diaminobenzidine reaction. The sections were dehydrated in a graded series of alcohols, cleared in xylene, and cover-slipped with Entellan (Merck, Darmstadt, Germany).

For simultaneous visualization of CGRP and galanin in the trigeminal ganglion, a double-immunofluorescent method was used. The sections were incubated for 24 hrs at room temperature with a mixture of rabbit anti-galanin (1:1000) and rabbit anti-CGRP serum (1:1000; Milab, Malmö, Sweden), then treated with a mixture of LissamineTM rhodamine B chloride-conjugated donkey anti-rabbit IgG (1:500 for galanin; Jackson Laboratories, Bar Harbor, ME, USA) and fluorescein isothiocynate-conjugated donkey anti-guinea pig IgG (1:100 for CGRP; Jackson Laboratories). The specificity of the primary antiserum used in this study has been described elsewhere (Winsky et al., 1989; Ichikawa and Helke, 1993).

Histomorphometry
Cell counts of immunoreactive and immunonegative neurons were made in the caudal one-third of the trigeminal ganglion. This portion has been identified as the mandibular division (Ichikawa et al., 1997). The mandibular division of each ganglion yielded a complete series of 60–70 sections. The numbers of immunoreactive and immunonegative neurons were counted in every tenth of the serial sections of the trigeminal ganglion (6 or 7 sections from each ganglion). For cell size analysis, the microscopic image (x215) of galanin-immunoreactive cell bodies was projected over a digitizer tablet by means of a drawing tube (Digitizer KW4620, Graphtec, Yokohama, Japan). The cross-sectional area of those cell bodies that contained the nucleolus was measured in every tenth section. Differences in the number and cell size distribution of galanin-immunoreactive neurons between control and experimental rats were analyzed by ANOVA and Student’s t test, respectively. For co-expression of galanin and CGRP, the numbers of neurons exhibiting galanin-immunoreactivity, CGRP-immunoreactivity, and both galanin-and CGRP-immunoreactivity were counted in representative sections. Differences in galanin-immunoreactive neurons between control and experimental rats were analyzed by two-way ANOVA and Fisher’s Protected Least Significant Difference for post hoc comparison at a significance level of p < 0.05.

All experiments complied with the regulations of the Animal Research Control Committee in accordance with The Guidelines for Animal Experiments of Okayama University Medical School, Government Animal Protection and Management Law (No. 105), and Japanese Government Notification on Feeding and Safekeeping of Animals (No. 6). All efforts were made to minimize the number and suffering of animals used.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
In the control group, the mandibular division of trigeminal ganglions contained a few galanin-immunoreactive neurons (Fig. 2aGo). In contrast, a marked increase of trigeminal ganglion neurons was observed after experimental tooth movement (Fig. 2bGo). The proportion of immunoreactive neurons among the total number of neurons in the mandibular division was 6.5 ± 0.7% (mean ± SE, n = 6) for the control (Fig. 3aGo). At 1 day after insertion of the elastic band, no significant difference was observed (6.8 ± 0.4%; n = 6) compared with that in the control. The proportion of immunoreactive neurons increased at 3 days (12.3 ± 1.9%; n = 6) after insertion of the elastic band (p < 0.001). The greatest increase was detected 5 days (24.3 ± 1.8%; n = 6) after the treatment (p < 0.0001) (Fig. 2bGo). Then, the proportion of immunoreactive neurons gradually decreased from 7 days (10.2 ± 0.6%; n = 6) (p < 0.05) and returned to normal levels at 14 days (7.0 ± 0.5%; n = 6), and 28 days (7.2 ± 1.1%; n = 6). The present cell size analysis demonstrated that galanin-immunoreactive neurons were mainly small in the control trigeminal ganglion (mean ± SE = 180.4 ± 8.9 µm2); 61.4 ± 6.9% of galanin-immunoreactive neurons demonstrated small cell bodies (< 200 µm2) (Fig. 3bGo), while 35.6 ± 9.8% of galanin-immunoreactive neurons were medium-sized (200–600 µm2). Large galanin-immunoreactive neurons were very rare in the trigeminal ganglion (> 600 µm2, made up 3.0 ± 1.0% of neurons). Three days after experimental tooth movement, many small and medium-sized trigeminal ganglion neurons showed galanin immunoreactivity, and the mean ± SE of immunoreactive cell sizes was 252.1 ± 8.1 µm2. At 5 days, medium-sized and large galanin-immunoreactive neurons markedly increased in number (Fig. 3bGo). As a result, galanin-immunoreactive neurons were of various sizes, with medium-sized neurons comprising the larger percentage of neurons (small, 31.3 ± 5.0%; medium-sized, 64.6 ± 3.1%; large, 4.1 ± 1.9%). Fourteen days after experimental tooth movement, the cell-size spectrum of galanin-immunoreactive neurons was similar to that of immunoreactive neurons in control animals (mean ± SE = 186.8 ± 12.5 µm2) (Fig. 3bGo). Small and medium-sized neurons constituted 58.7 ± 8.2% and 39.1 ± 6.0% of galanin-immunoreactive populations at 14 days. Only 2.2 ± 4.4% of immunoreactive neurons had large cell bodies.


Figure 2
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  		Figure 2. Galanin-immunoreactive trigeminal ganglion neurons (arrows) in the mandibular division of (a) controls and (b) 5 days after experimental tooth movement. Bar = 50 µm (a).

 

Figure 3
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  		Figure 3a. Change in the proportion of galanin-immunoreactive neurons in the trigeminal ganglion in each experimental stage after experimental tooth movement (n = 6 for each stage). Each value represents the mean ± SE. *Significant difference in the proportion of GAL-positive neurons at the p < 0.05 level.

Figure 3b. Change in the number of galanin-immunoreactive trigeminal ganglion neurons in different cell size ranges in controls, at 5 days, and at 14 days after experimental tooth movement (n = 6). Each value represents the mean ± SE. *Significant difference in the number of galanin-immunoreactive neurons at the p < 0.05 level.

 
Our double-immunofluorescence method demonstrated co-expression of galanin and CGRP (Fig. 4Go). Half of the trigeminal ganglion neurons in the mandibular region were immunoreactive for CGRP in the control (mean ± SE = 41.7 ± 2.1%) and following experimental tooth movement throughout the experimental period (3 days, 51.0 ± 9.2%; 5 days, 45.5 ± 3.6%; 7 days, 45.3 ± 2.5%; 14 days, 43.7 ± 3.6%). Galanin-immunoreactive trigeminal ganglion neurons mostly co-expressed CGRP immunoreactivity in control (85.4 ± 0.2%) (Figs. 4a–4cGo) and experimental rats (Figs. 4d–4iGo). At 3, 5, and 14 days after experimental tooth movement, 85.4% ± 1.7%, 94.8% ± 1.3%, and 90.5% ± 0.6% of galanin-immunoreactive neurons co-expressed CGRP immunoreactivity, respectively. Therefore, the number of trigeminal ganglion neurons that co-expressed these substances increased at 3 days (mean ± SE of co-expressing neuron proportion among trigeminal ganglion neurons = 10.4 ± 0.2%) and 5 days (23.0 ± 4.8%) (Figs. 4d–4fGo), and tended to return to the control level (5.8% ± 0.5%) at 14 days (6.3 ± 3.6%) (Figs. 4g–4iGo). The difference between control and experimental trigeminal ganglions at 3 days (p < 0.001) and 5 days (p < 0.0001) was highly significant.


Figure 4
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  		Figure 4. Immunofluorescent micrographs for CGRP (a,d,g), galanin (b,e,h), and both (c,f,i) of the trigeminal ganglion of controls (a,b,c), and at 5 (d,e,f) and 14 (g,h,i) days after experimental tooth movement. In the controls and at 14 days, galanin immunoreactivity was observed mainly in small neurons, whereas at 5 days, medium-sized to large neurons also expressed galanin. Arrows point to CGRP and galanin-immunoreactive neurons. Arrowheads indicate CGRP-positive but galanin-negative neurons. Bar = 10 µm (i). All panels are at the same magnification.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Our previous study demonstrated that experimental tooth movement dramatically increased galanin-immunoreactive nerve fibers in the periodontal ligament (Deguchi et al., 2003). Galanin immunoreactivity was detected in numerous free nerve endings and perivascular endings. However, it has been unclear whether experimental tooth movement resulted in the sprouting of galanin-immunoreactive nerve fibers, or the induction of galanin in normally negative neurons, or both. The present study demonstrated an increase in galanin-immunoreactive neurons in the trigeminal ganglion during experimental tooth movement compared with control. Therefore, it is suggested that these nerve fibers originate at least partly from the trigeminal ganglion and peripherally release galanin during experimental tooth movement. However, the possibility that galanin-immunoreactive nerve fibers during experimental tooth movement have an autonomic origin derived from the superior cervical ganglion could not be excluded. There was no significant difference in the number of galanin-immunoreactive neurons between the six-week-old and 10-week-old rats in the control trigeminal ganglions. A previous investigation that compared the expression of galanin-immunoreactive neurons in the facial nucleus between adult and aged rats after facial nerve transection detected no significant change in the galanin-immunoreactive neurons during 20 mos of the experimental period (Johnson and Duberley, 1998). In this previous study, the location of the analyzed neurons and the age of the rats were different from those in our study. However, we strongly believe that there was no significant age-related change in galanin immunoreactivity in this study.

In the trigeminal ganglion, the cell size spectra of galanin-immunoreactive neurons differed between normal and experimental animals. In normal animals, galanin immunoreactivity was mainly detected in small trigeminal ganglion neurons. Five days after experimental tooth movement, however, many medium-sized and large trigeminal ganglion neurons showed galanin immunoreactivity. In addition, our double-immunofluorescence method demonstrated that galanin-immunoreactive neurons mostly co-expressed CGRP immunoreactivity in normal and experimental trigeminal ganglions. Previous studies demonstrated that CGRP-immunoreactive neurons have both unmyelinated and myelinated axons (Kakudo et al., 1988; Ishida-Yamamoto and Senba, 1990). Small CGRP-immunoreactive neurons were unmyelinated, whereas medium-sized and large CGRP-immunoreactive neurons showed finely myelinated axons. Therefore, it is likely that medium-sized and large CGRP-immunoreactive neurons with finely myelinated axons may show galanin immunoreactivity during experimental tooth movement. It is known that the expression of galanin in sensory neurons is regulated by neurotrophins (Verge et al., 1995; Shadiack et al., 2001). Intraperitoneal injection of nerve growth factor (NGF) reduced the number of galanin mRNA-positive neurons in the dorsal root ganglion after sciatic nerve transection (Shadiack et al., 2001). In addition, treatment with NGF antibody decreased galanin mRNA in the sensory ganglion (Verge et al., 1995). Therefore, it is possible that experimental tooth movement caused the change of NGF level in the periodontal ligament and in the trigeminal ganglion, and thereby resulted in the change of the mRNA levels of galanin expression. This idea may be supported by the present finding that galanin was increased in CGRP-containing trigeminal neurons, because CGRP-containing neurons are sensitive to NGF for their CGRP expression and axonal sprouting (Byers et al., 1992; Amann et al., 1996). In this study, however, the content of NGF in the periodontal ligament was not investigated. Further studies are necessary before we will know whether neurotrophin is associated with the increase of galanin after experimental tooth movement.

CGRP and galanin are known to have nociceptive functions in the spinal cord (Ju et al., 1987; Cridland and Henry, 1988; Ryu et al., 1988; Wiesenfeld-Hallin et al., 1989). CGRP can enhance nociceptive inputs to secondary neurons (Cridland and Henry, 1988; Ryu et al., 1988), while galanin has a suppressive effect on nociceptive transmission in the cord (Wiesenfeld-Hallin et al., 1989). Therefore, the increased galanin-immunoreactive neurons and co-expression of galanin and CGRP suggest that galanin is associated with the modulation of nociceptive information. In addition, CGRP has been suggested to affect bone remodeling during experimental tooth movement (Kvinnsland and Kvinnsland, 1990; Saito et al., 1991). This peptide is known to suppress differentiation of osteoclasts (D’Souza et al., 1986; Zaidi et al., 1987; Mullins et al., 1993), and may promote bone formation (Bjurholm et al., 1990; Ballica et al., 1999). Although the effect of galanin on osteoclasts, osteoblasts, or fibroblasts in the periodontal ligament has not been reported previously, tissue remodeling has been shown to be very active from 3 to 5 days after insertion of an elastic band (Takano-Yamamoto et al., 1992; Yamashiro et al., 2000). The most intense increase in galanin-immunoreactive nerve fibers in the periodontal ligament was observed 3 days after experimental tooth movement (Deguchi et al., 2003). In this study, the greatest increase of galanin-immunoreactive neurons in the trigeminal ganglion was observed 5 days after the insertion of an elastic band. Therefore, it may be that galanin synthesis is up-regulated in the trigeminal primary neurons innervating the periodontal ligament, and the peripherally transported galanin plays a role in periodontal ligament remodeling. Further investigations are necessary to elucidate differences in the expression of galanin between the trigeminal ganglion and the periodontal ligament.

In conclusion, we have described galanin expression in the trigeminal ganglion during experimental tooth movement. This treatment induced galanin immunoreactivity in normally immunonegative trigeminal ganglion neurons. These neurons mostly co-expressed CGRP immunoreactivity. The present study suggests that galanin may play a role in periodontal ligament remodeling.


   ACKNOWLEDGMENTS
 
This study was supported by Grants-in-Aid for Scientific Research from the Japan Society for the Promotion of Science.

Received April 26, 2005; Last revision February 19, 2006; Accepted February 21, 2006


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 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
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