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Biological

Expression of MMP-8 and MMP-13 mRNAs in Rat Periodontium during Tooth Eruption

M. Tsubota1, Y. Sasano2,*, I. Takahashi3, M. Kagayama2 and H. Shimauchi1

1 Division of Periodontics and Endodontics, Tohoku University Graduate School of Dentistry, Sendai 980-8575, Japan;
2 Division of Oral Molecular Biology, Tohoku University Graduate School of Dentistry, Sendai 980-8575, Japan; and
3 Division of Orthodontics, Tohoku University Graduate School of Dentistry, Sendai 980-8575, Japan;

Correspondence: * corresponding author, sasano{at}anat.dent.tohoku.ac.jp


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The present study was designed to investigate mRNA expression of matrix metalloproteinase-8 (MMP-8) and MMP-13 in forming periodontium during tooth eruption in the rat. RT-PCR for the decalcified paraffin sections indicated expression of MMP-8 and MMP-13 in the periodontal tissues. In situ hydridization demonstrated expression of MMP-8 in osteoblasts, osteocytes, periodontal ligament cells, cementoblasts, and cementocytes along with collagen types I and III. In contrast, transcripts of MMP-13 were confined to a small population of osteoblasts and osteocytes in alveolar bone. The results suggested that MMP-8 may be involved in remodeling the periodontium during tooth eruption, and its expression may be coordinated with that of collagen types I and III, whereas the participation of MMP-13 may be rather limited.

Key Words: collagenase • collagen • periodontal ligament • in situ hybridization • RT-PCR


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Periodontal ligaments sustain the roots of teeth within maxillary and mandibular bones and buffer the mastication stress on the tooth. Major extracellular components of the periodontal ligaments are collagen types I and III (Takita et al., 1987; Huang et al., 1991). The collagenous extracellular matrix is turned over during remodeling of periodontal ligaments, e.g., in case of tooth eruption (MacNeil et al., 1998) or tooth movement with orthodontic force (Nakagawa et al., 1994; Karimbux and Nishimura, 1995). However, enzymes which degrade the collagens of periodontal ligaments are not known.

The matrix metalloproteinases (MMPs) are thought to play a central role in the breakdown of extracellular matrix, which is essential for embryonic development, morphogenesis, and tissue remodeling (Birkedal-Hansen et al., 1993; Nagase and Woessner, 1999). Collagenases are the only members of the MMPs family that degrade native fibrillar collagens of types I, II, and III (Gack et al., 1995; Franchimont et al., 1997; Johansson et al., 1997; Woessner and Nagase, 2000). MMP-1, -8, and -13 comprise the collagenase subfamily in humans, while only two of them, MMP-8 and -13, had been identified in rodents (Jeffrey, 1998a; Woessner and Nagase, 2000) until a mouse orthologue of human MMP-1 was recently reported (Balbín et al., 2001).

MMP-13 is the only interstitial collagenase that has been suggested to degrade collagens in connective tissues in rats (Jeffrey, 1998a,b). MMP-8 was originally thought to be confined to neutrophils (Tschesche and Pieper, 1998; Woessner and Nagase, 2000), but recent studies indicate that it may be expressed in other cell types, such as articular chondrocytes (Cole et al., 1996), synovial fibroblasts and endothelial cells (Hanemaaijer et al., 1997), odontoblasts and dental pulp cells (Palosaari et al., 2000), and osteoblasts and osteocytes (Sasano et al., 2002). The present study was designed to investigate mRNA expression of MMP-13 and -8 in rat periodontal ligaments and other periodontal tissues during tooth eruption, by means of reverse transcription followed by polymerase chain-reaction (RT-PCR) and in situ hybridization. Cell types which express collagenous matrix molecules were identified by in situ hybridization for collagen types I and III.


   MATERIALS & METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Preparation of Tissue
The principles of laboratory animal care (NIH publication no. 86-23, revised 1985) were followed, as were specific national laws and animal protocols that were institutionally approved by Tohoku University. Wistar male rats at 2, 3, 4, and 6 wks of age were used. Rats were fixed with 4% paraformaldehyde with 0.5% glutaraldehyde in 0.1 M phosphate buffer, pH 7.4, by perfusion through the aorta. Maxillae were resected and kept in the fixative overnight at 4°C. The fixed specimens were decalcified in 10% EDTA in 0.01 M phosphate buffer, pH 7.4, for 3-7 wks at 4°C. The EDTA solution was autoclaved before use. After dehydration through a graded series of ethanol, the tissues were embedded in paraffin (Sasano et al., 1996, 2002). Serial sections 5 µm thick were cut, and the adjacent sections were stained with hematoxylin-eosin, or processed for Section-RT-PCR or in situ hybridization.

Section-RT-PCR
The sections were deparaffinized and washed in phosphate-buffered saline (PBS), immersed in 0.2N HCl for 20 min, and incubated in proteinase K (20 µg/mL; Roche, Mannheim, Germany) in PBS for 30 min at 37°C after being washed in PBS. The sections were then treated with DNase I (0.25 U/µL; Roche) for 60 min at 37°C and proteinase K (20 µg/mL; Roche) for 60 min at 37°C for digestion of the DNase I. After being washed in PBS and 100% ethanol and being air-dried, the maxillary periodontal regions were excised from the sections and homogenized in water.

cDNA was synthesized with use of the homogenized solution primed with 1.0 µM of random primers (Invitrogen, Carlsbad, CA, USA) in the presence of Sensiscript Reverse Transcriptase (QIAGEN; Hilden, Germany) in a reverse transcription buffer. For cDNA amplification, 1.0 µL of reverse-transcription products was incubated in the presence of 20 pmol of two specific primers (Fig. 1Go), 1.5 mM MgCl2, 0.2 mM of the 4 dNTPs (Invitrogen), and 0.05 U of Taq polymerase in a reaction buffer (Invitrogen). The reaction mixture was subjected to one cycle of denaturation for 3 min 50 sec at 95°C, followed by 40 cycles of an amplification sequence that consisted of denaturation for 70 sec at 95°C, annealing for 70 sec at 60°C for MMP-8, 59°C for MMP-13, and 57°C for glyceraldehyde-3-phosphate dehydrogenase (GAPDH) and extension for 1 min 30 sec with an additional 8 min 30 sec for the last cycle. The solution of the homogenized sections without reverse transcription (non-RT) was used for a negative control. Total RNA extracted from embryonic rat limbs was used for a positive control.


Figure 1
Figure 1
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  		Figure 1. Oligonucleotide primers used for Section-RT-PCR (upper). Section-RT-PCR of rat maxillary periodontium in weeks 3 (W3) and 4 (W4) (lower). Gene expression of MMP-8, MMP-13, and GAPDH is identified. Negative controls (non-RT) do not produce bands visible on gels. Positive controls (total RNA of embryonic rat limbs) show the corresponding bands.

 
Following amplification, equal amounts of PCR products were size-separated by electrophoresis through a 4.0% agarose gel (NuSieve GTG agarose: BMA, Rockland, ME, USA) and visualized by ethidium bromide staining and ultraviolet transillumination. All samples were amplified at least twice on different occasions to control for any variations in the PCR technique. Images of the stained gels were captured by means of the Electrophoresis Documentation and Analysis System (Kodak, Rochester, NY, USA).

Preparation of RNA Probes
Digoxigenin (DIG)-labeled single-strand RNA probes were prepared by means of the DIG RNA labeling kit (Roche) according to the manufacturer’s instructions.

Fragments encoding rat pro-{alpha}1(III) collagen (1462 bp-2097 bp: GenBank X70369), rat MMP-8 (171bp-1253bp: GenBank AJ007288), and rat MMP-13 (1547bp-2411bp: GenBank M60616, M36452) were obtained from the total RNA of embryonic rat limbs by RT-PCR and subcloned into the pCR II TOPO (Invitrogen, Carlsbad, CA, USA). A fragment encoding rat pro-{alpha}1(I) collagen (2838bp-4329bp: GenBank Z78279) was obtained from the total RNA of rat skin by RT-PCR and subcloned into the pT7/T3-a18 plasmid (Life Technologies, Grand Island, NY, USA). Oligonucleotide primers used for the RT-PCR are shown in Fig. 2Go. The cDNA was verified by digestion with restriction enzymes and confirmed by dideoxynucleotide sequencing. RNA probes were generated as indicated in Fig. 2Go.


Figure 2
Figure 2
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  		Figure 2. Oligonucleotide primers to prepare for RNA probes (upper). RNA polymerases and restriction enzymes used for RNA probes (middle). In situ hybridization for COL I (a-d) and COL III (e-h) during root formation and eruption of maxillary first molars (lower). (a,e) Week 2. (b,c,f,g) Week 4. (d,h) Week 6. Arrowheads in (c) and (g) indicate hybridization signals. B, alveolar bone; P, periodontal ligaments; C, cementum; D, dentin. Bars = 10 µm (a,e); 20 µm (b,d,f,h); 5 µm (c,g).

 
In situ Hybridization
The protocol used in the present study has been reported previously (Sasano et al., 1996, 2002) and is only briefly described here. The sections were deparaffinized and washed in phosphate-buffered saline (PBS), immersed in 0.2 N HCl for 20 min, and, after being washed in PBS, incubated in proteinase K (20 µg/mL; Roche) in PBS for 30 min at 37°C. After being washed, the sections were dipped in 100% ethanol and dried in air. The sections were then incubated with the anti-sense or sense probes (400 ng/mL) in a hybridization mixture for 16 hrs at 45°C. After being washed, the sections were treated with RNase (Type 1a, 20 µg/mL; Sigma, St. Louis, MO, USA) for 30 min at 37°C. After being washed, the hybridized probes were detected immunologically by means of the Nucleic Acid Detection Kit (Roche), counterstained with methyl green, and mounted.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Section-RT-PCR
Sections used for RT-PCR contained molar roots, periodontal ligaments, and alveolar bone. Gene expressions of MMP-8 and MMP-13 in the periodontal tissues were identified with Section-RT-PCR. Negative controls (non-RT) did not produce bands visible on gels, while positive controls (total RNA of embryonic rat limbs) showed the corresponding bands (Fig.1Go).

In situ Hybridization
The investigation was focused on maxillary first molars and surrounding periodontal tissue. The crown formation of the first molar was completed and the root formation and eruption started in week 2. The molar continued to erupt, with growing roots in week 3, and root elongation and eruption were completed in week 4.

The gene expression detected by the Section-RT-PCR was localized by in situ hybridization. The results are summarized in the TableGo.


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  		Table. The mRNA Expression Patterns Demonstrated with in situ Hybridization
 
The pro-{alpha}1(I) collagen (COL I) signal was strong in odontoblasts and weak in cementoblasts and cemenocytes throughout the study. In osteoblasts, osteocytes, and periodontal ligament cells, the strong signal was identified and the intensity was highest in weeks 3 and 4 and decreased in week 6 (Figs. 2a-2dGo).

Pro-{alpha}1(III) collagen (COL III) was weakly expressed in odontoblasts, cementoblasts, cementocytes, osteoblasts, and osteocytes throughout the study. Only in periodontal ligament cells was the strong signal identified, and the intensity was highest in weeks 3 and 4 and decreased in week 6 (Figs. 2e-2hGo).

MMP-8 transcripts were weakly demonstrated in odontoblasts, cementoblasts, and cementocytes throughout the study. In osteoblasts, osteocytes, and periodontal ligament cells, the strong signal was identified and the intensity was highest in weeks 3 and 4 and decreased in week 6 (Figs. 3a-3dGo).


Figure 3
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  		Figure 3. In situ hybridization for MMP 8 (a-d) and MMP 13 (e-h) during root formation and eruption of maxillary first molars. (a,e) Week 2. (b,c,f,g) Week 4. (d,h) Week 6. The insert in (f) is an image with a higher magnification of the enclosed region. Arrowheads in (c), (e) and (f) indicate hybridization signals. B, alveolar bone; P, periodontal ligaments; C, cementum; D, dentin. Bars = 10 µm (a,e); 20 µm (b,d,f,h); 5 µm (c,g).

 
Hybridization signal for MMP-13 was hardly detectable in odontoblasts, cementoblasts, cementocytes, and periodontal ligament cells (Figs. 3e-3hGo). The mRNA transcripts were confined to a small population of osteoblasts and osteocytes in alveolar bone (Figs. 3e, 3fGo).

Controls for in situ Hybridization
No hybridization signal was identified in the adjacent sections processed with control sense RNA probes.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
A previous study reported that MMP-13 was identified in sulcular epithelial cells, gingival fibroblasts, and monocyte/macrophage-like cells in periodontal tissues of adult and localized juvenile periodontitis patients, whereas MMP-8 was detected in neutrophils and sulcular epithelial cells (Tervahartiala et al., 2000). MMP-8 and -13 may be the major collagenolytic enzymes that degrade extracellular matrices of the inflamed periodontal tissue. In contrast, little is known about involvement of these enzymes in the physiological remodeling of periodontal tissues during tooth eruption.

Extraction of RNA from periodontal tissues requires complicated procedures, such as collecting periodontal tissue cells from the root surfaces of extracted teeth and amplifying the cells in culture (Bolcato-Bellemin et al., 2000). Culturing, on the other hand, may change the gene expression profiles of the cells. To overcome these problems, we utilized decalcified paraffin sections and processed the excised region of periodontal tissues for Section-RT-PCR. Our previous study has shown that RNA is well-preserved after fixation with a mixture of glutaraldehyde and paraformaldehyde and subsequent paraffin-embedding (Sasano et al., 1996). This method is especially beneficial for the identification and collection of the particular region of calcified tissues for RT-PCR, in which homogenization and extraction of hard calcified tissues for RNA would otherwise be inevitable. The Section-RT-PCR performed in the present study demonstrated mRNA expression of MMP-8 and MMP-13 in the rat periodontal tissue during tooth eruption.

We applied in situ hybridization to localize the mRNA expression of MMP-8 and -13 detected with the Section-RT-PCR. The results indicated that MMP-8 transcripts are expressed in osteoblasts, osteocytes, periodontal ligament cells, cementoblasts, cementocytes, and odontoblasts during physiological development of periodontal tissues, whereas MMP-13 is confined to a small population of osteoblasts and osteocytes in alveolar bone. Expression of MMP-8 was particularly intense in osteoblasts, osteocytes, and periodontal ligament cells in weeks 3 and 4, during which alveolar bone and periodontal ligaments were being remodeled with tooth eruption. This is the first report indicating expression of MMP-8 in periodontal ligament cells, cementoblasts, and cementocytes. Also, the findings of MMP-8 expression in osteoblasts and osteocytes in alveolar bone are in agreement with our recent report about embryonic bone development (Sasano et al., 2002). The results of the present study suggested that MMP-8 may be involved in remodeling of periodontal tissues during tooth eruption, whereas confined expression of MMP-13 may represent limited participation of this enzyme.

The present and previous studies demonstrate gene expression of COL I in osteoblasts, osteocytes, periodontal ligament cells, cementoblasts, cementocytes, and odontoblasts (Nakagawa et al., 1994; Sasano et al., 2001). In contrast, the cells responsible for production of type III collagen in periodontal tissues have not been identified, since only immunolocalization of type III collagen in periodontal ligaments has previously been described (Takita et al., 1987). We indicated for the first time that mRNA of COL III is expressed in several periodontal tissue types, i.e., periodontal ligament cells, cementoblasts, cementocytes, and osteoblasts and osteocytes in alveolar bone. In particular, periodontal ligament cells expressed COL III intensely during the peak time of root formation and periodontal tissue remodeling in weeks 3 and 4.

The most intense expression of MMP-8 in the periodontal ligament was co-localized with those of COLs I and III. Periodontal ligament cells may be involved in both production and degradation of collagenous matrices by expressing COLs I, III, and MMP-8 during the formation of periodontal tissues. Cathepsins B and L have been localized in mature rat periodontal ligaments (Takeyama et al., 2001). Cultured human periodontal ligament cells express cathepsins B and L (Goseki et al., 1996). MMPs and cathepsins may cooperate in remodeling periodontal ligaments and other periodontal tissues.

Although all the human collagenases, MMP-1, -8, and -13, cleave collagen types I, II, and III, MMP-1 prefers type III collagen, MMP-8 prefers type I, and MMP-13 prefers type II collagen (Cawston, 1998; Woessner and Nagase, 2000). Since rat MMP-1 has not been identified (Jeffrey, 1998a; Woessner and Nagase, 2000), some of the functions of MMP-1 in humans may involve MMP-8 and/or MMP-13 in rats.

The present study demonstrated that MMP-8 is expressed by periodontal ligament cells, osteoblasts, osteocytes, cementoblasts, cementocytes, and odontoblasts, while expression of MMP-13 is confined to a small population of osteoblasts and osteocytes in alveolar bone during the periodontium formation. Furthermore, the most intense expression of MMP-8 in periodontal ligament is co-localized with those of COLs I and III. MMP-8 may play an important role in organization of collagenous matrices in the forming periodontal ligaments and other periodontal tissues during rat tooth eruption. Since the expression patterns of collagenases between humans and rodents differ from each other, it is possible that, in humans, other collagenases (especially interstitial collagenase MMP-1) are responsible for the respective functions in humans (Jeffrey, 1998b; Woessner and Nagase, 2000). The differences between species remain to be confirmed in future studies.


   ACKNOWLEDGMENTS
 
We thank Dr. Hiroshi Horiuchi, Professor Emeritus at Tohoku University, for his constructive suggestions to this study. We also thank Mr. Masami Eguchi and Mr. Yasuto Mikami, Division of Oral Molecular Biology, Tohoku University Graduate School of Dentistry, for their excellent assistance in this study. This work was supported in part by a grant-in-aid (13671893) from the Ministry of Education, Science, Sports and Culture of Japan.

Received for publication January 2, 2002. Revision received May 28, 2002. Accepted for publication July 8, 2002.


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 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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Journal of Dental Research, Vol. 81, No. 10, 673-678 (2002)
DOI: 10.1177/154405910208101004
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