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Chronic Periodontal Disease Is Associated with Single-Nucleotide Polymorphisms of the Human TLR-4 Gene

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Chronic Periodontal Disease Is Associated with Single-Nucleotide Polymorphisms of the Human TLR-4 Gene Genes and Immunity (2005) 6, 448–451 & 2005 Nature Publishing Group All rights reserved 1466-4879/05 $30.00 www.nature.com/gene BRIEF COMMUNICATION Chronic periodontal disease is associated with single-nucleotide polymorphisms of the human TLR-4 gene NWJ Schro¨der1,5, D Meister1, V Wolff1, C Christan2, D Kaner3, V Haban1, P Purucker3, C Hermann4, A Moter1,UBGo¨bel1 and RR Schumann1 1Institute for Microbiology and Hygiene, Charite´ University Medical Center Berlin, Berlin, Germany; 2Private Dental Office, Berlin, Germany; 3Department of Periodontology and Synoptic Dentistry, Charite´ University Medical Center, Berlin, Germany; 4Biochemical Pharmacology, Department of Biology, University of Konstanz,Konstanz, Germany Periodontitis is an inflammatory disease affecting the connective tissue surrounding the teeth leading to tooth loss. Pathogens associated with periodontitis interact with Toll-like receptors (TLRs) to induce cytokines causing and aggravating disease. We screened 197 individuals suffering from generalized periodontitis for the presence of Asp299Gly and Thr399Ile of TLR-4 as well as Arg753Gln of TLR-2 in comparison to matched controls. Single-nucleotide polymorphisms (SNPs) of TLR-4 were elevated among patients (odd’s ratio 3.650, 95% CI 1.573–8.467, Pp0.0001), while no difference was observed for TLR-2. TLR-4 SNPs were correlated with chronic periodontitis (odd’s ratio 5.562, 95% CI 2.199–14.04, Pp0.0001), but not with aggressive periodontitis. This observation was confirmed employing a group of periodontally healthy probands over 60 years of age. These data demonstrate that genetic variants of TLR-4 may act as risk factors for the development of generalized chronic periodontitis in humans. Genes and Immunity (2005) 6, 448–451. doi:10.1038/sj.gene.6364221; published online 5 May 2005 Keywords: periodontitis; innate immunity; Toll-like receptors; single-nucleotide polymorphisms; disease susceptibility Periodontitis is an inflammatory disease affecting gingiva, Porphyromonas gingivalis, have been frequently recovered periodontal ligament, cementum and alveolar bone.1 The from periodontal lesions.6,7 There is evidence that innate major symptoms are formation of periodontal pockets, immune responses aggravate periodontal disease, since bleeding and destruction of connective tissue attachment, the proinflammatory cytokines IL-1 and TNF-a, reported also referred to as attachment loss, eventually leading to to be elevated in patients,8 act synergistically, ie in tooth loss.1 Periodontitis over-exceeds dental caries as causing bone resorption.9 The release of IL-1 and TNF-a leading cause of tooth loss worldwide,2 thus being a major by monocytes and macrophages is induced via a path- burden for health care systems. It is a common disease way involving the family of Toll-like receptors (TLRs).10 with an estimated prevalence of approx 50% among TLR-4 recognizes lipopolysaccharide (LPS), a partial adults, with 10–30% displaying severe forms of disease structure of Gram-negative bacteria, including period- characterized by an involvement of X30% of the teeth ontal pathogens.10 Recent data suggest that P. gingivalis, referred to as generalized periodontitis.3,4 Chronic period- in contrast to other Gram-negative bacteria, exhibits an ontitis (CP), progressing slowly and being predominantly untypical variant of LPS interacting with TLR-4, but also found among the elderly, is distinguished from aggressive TLR-2,11,12 a receptor generally recognizing cell wall periodontitis (AP), where rapid progression of attachment compounds distinct from LPS, such as lipoproteins.13 loss is mainly found in young adults.5 However, aggres- Thus, TLR-2 may be involved in innate immune sive courses of disease may also occur in elder patients.5 responses against periodontal pathogens. Expression of Attachment loss in periodontitis is considered to be both, TLR-2 and -4, has been shown to be increased in a result of both bacterial infection of subgingival macrophages as well as in gingival fibroblasts within tissue as well as host factors primarily directed against inflamed periodontal tissue.14 Furthermore, TLR-4-defi- these pathogens. Gram-negative anaerobe rods, ie cient C3H/HeJ mice exhibit reduced bone resorption in a periodontitis model,15 further indicating that TLRs may play a crucial role in periodontitis. Correspondence: Professor RR Schumann, Institut fu¨r Mikrobiologie und Several studies investigated the impact of single- Hygiene, Charite´—Universita¨tsmedizin Berlin, Dorotheenstrasse 96, nucleotide polymorphisms (SNPs) within genes encod- D-10117 Berlin, Germany. E-mail: [email protected] ing for proinflammatory cytokines on periodontal health, 5Current address: Pediatrics Infectious Diseases, Cedars Sinai Medical Center, Los Angeles 90048, CA, USA. ie SNPs within the IL-1 gene cluster, which lead to Received 3 January 2005; revised and accepted 6 April 2005; higher levels of IL-1b, describing an association of the published online 5 May 2005 occurrence of an SNP with CP and AP, respectively.16,17 TLR-4 polymorphisms in human periodontitis NWJ Schro¨der et al 449 Within the TLR-4 gene two cosegregating SNPs, Asp299Gly was found in two, Thr399Ile in three patients, Asp299Gly and Thr399Ile have been described leading but none of the controls exhibited one of these SNPs. to decreased cytokine release by epithelial cells upon Thus, 43 patients suffering from generalized period- LPS-stimulation in vitro, and are associated with hypo- ontitis displayed TLR-4 variants as compared to 14 found responsiveness to inhaled LPS, as well as with Gram- in the controls (OR 3.650 95% CI 1.573–8.467, P-value negative sepsis, septic shock and Legionnaire’s disease p0.0001). (reviewed in Schro¨der and Schumann18). Within the gene Since CP and AP are regarded as different disease encoding for human TLR-2, an SNP (Arg753Gln) was entities, we stratified the patients for clinical course of described diminishing inflammatory responses to TLR-2 disease. Patients suffering from CP (n ¼ 116) displayed a ligands in vitro and occurring at a frequency of higher frequency of the cosegregating SNPs as compared approximately 10% among Caucasians.19,20 to controls (OR 4.291 95% CI 1.669–11.03, P-value 0.002), To find out whether the genetic variations of TLR-4 while no significant difference was found for AP (n ¼ 81, and -2 influence periodontal disease susceptibility, we Table 2). Rare genotypes of TLR-4 were found exclu- investigated 197 patients suffering from periodontitis, sively within patients suffering from CP, strengthening both AP and CP, for the presence of the SNPs Asp299Gly the association of TLR-4 variants with this clinical picture and Thr399Ile of TLR-4 as well as Arg753Gln of TLR-2. (OR 5.562 95% CI 2.199–14.04, P-value 0.0001). In contrast Inclusion criteria for patients were clinical attachment to the observations made for TLR-4, we did not observe loss (CAL) of X3 mm affecting X30% of the teeth any significant association of the TLR-2 SNP with consistent with moderate to severe generalized period- periodontitis (OR 0.588 95% CI 0.270–1.280, P-value ontitis. Patients were stratified for clinical presentation of 0.2467, Table 2), and this was not affected by stratification AP and CP according to the classification system of the patients for CP and AP. introduced by the American Academy of Periodontology Severe CP is a frequent disease occurring at 10–30% in 1999.5 Patients were also included in the AP group among different populations.3 Although the control when there was clinical evidence for rapid disease probands did not have a history of periodontitis at the progression. Mean CAL of all patients was 4.39 mm time of inclusion in the study, it cannot be excluded that (71.23 mm), with 4.07 mm (71.06 mm) for CP and they will develop this disease later. Thus, we aimed at 5.45 mm (71.19 mm) for AP patients. The patients’ strengthening our results by comparing the frequencies characteristics are shown in Table 1. We found the of TLR-SNPs among CP-patients with controls being combined Asp299Gly/Thr399Ile genotype of TLR-4 in 38 X60 years old having X20 teeth with p1 mm CAL. of the 197 patients examined (19.29% of all individuals, Among our control population, we identified 111 allele frequency 9.64%, Table 2). This frequency was individuals displaying these characteristics, and 75 could significantly higher as compared to matched controls, be matched with CP-patients regarding gender and where 14 individuals displayed this genotype (OR 3.124 smoking-status, with all individuals being nonsmokers. 95% CI 1.633–5.976, P-value 0.0005, Table 2). No Here, we observed a higher frequency of TLR-4 SNPs individuals exhibiting SNPs in a homozygous state were among the CP-patients as compared to these controls identified. A Hardy–Weinberg test in combination with a confirming our previous results (OR 4.814, 95% CI 1.526– w2 test was performed, showing that these frequencies 15.19, P-value 0.007, Table 3), while there was no were in line with the Hardy–Weinberg equilibrium significant association with TLR-2 (data not shown). (P-values 0.3255 and 0.8749 for patients and controls, This association was highly significant when all TLR-4 respectively). Some patients displayed rare genotypes variants were taken into account (OR 6.022, 95% CI with Asp299Gly or Thr399Ile occurring separately: 1.938–18.72, P-value 0.0011). Table 1 Composition of the patient and control group studied Periodontitis cases Matched controls n Mean age (years) Range Male (%) Smoker (%) n Mean age (years) Range Male (%) Smoker (%) Total 197 49.77711.95 22–81 43.2 34.5 197 43.71716.03 22–83 43.2 34.5 CPa 116 57.0778.82 40–81 38.8 36.2 116 55.0710.53 40–83 38.8 36.2 APb 81 39.3176.94 22–54 49.4 32.1 81 27.5274.48 22–39 49.4 32.1 aChronic periodontitis.
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