| |
|
|
| Year : 2006 | Volume
: 17
| Issue : 3 | Page : 114-6 |
|
| Expression of Toll-like receptors 2 and 4 in gingivitis and chronic periodontitis. |
|
|
SM Sarah, S Tamilselvan, S Kamatchiammal, R Suresh
Department of Periodontics, Sri Ramachandra Medical College & Research Institute, Porur, Chenai, India
Click here for correspondence address and email
|
|
 |
|
 Abstract | | |
Periodontal disease is the major cause of adult tooth loss and is commonly characterized by a chronic inflammation caused by infection by oral bacteria. Members of Toll-like receptor (TLR) family recognize conserved microbial structures, such as bacterial lipopolysaccharides, and activate signaling pathways that result in immune responses against microbial infections. The aim of the present study was to assess the mRNA expression of TLR-2 and TLR-4 in gingivitis and chronic periodontitis. Gingival tissue samples were collected from patients with chronic periodontitis, gingivitis, and healthy controls. Total RNA was extracted and RT-PCR was done for TLR-2 and TLR-4. The results showed that TLR-2 was significantly increased in gingivitis compared to TLR-4 expression and decreased in chronic periodontitis. Keywords: TLR-2. TLR-4, chronic periodontitis, gingivitis
How to cite this article:
Sarah S M, Tamilselvan S, Kamatchiammal S, Suresh R. Expression of Toll-like receptors 2 and 4 in gingivitis and chronic periodontitis. Indian J Dent Res 2006;17:114 |
How to cite this URL:
Sarah S M, Tamilselvan S, Kamatchiammal S, Suresh R. Expression of Toll-like receptors 2 and 4 in gingivitis and chronic periodontitis. Indian J Dent Res [serial online] 2006 [cited 2023 Sep 28];17:114. Available from: https://www.ijdr.in/text.asp?2006/17/3/114/29879 |
| Introduction | |  |
Periodontal disease consists of a group of infections that lead to inflammation of gingiva to destruction of periodontal tissues [1]. The current disease paradigm for the manifestation of periodontitis, involves both the bacterial and host components. In particular, evidence implicating a pathogenic role for a group of gram negative anaerobes including the species Porphyromonas gingivali has accumulated [2]. The immune response to microbial pathogens relies on both innate and adaptive components. A primary challenge to the innate immune system is the discrimination of a large number of receptors which has been met by the evolution of a variety of receptors that recognize conserved motifs on pathogens called the Toll-like receptors (TLR), homologous of the fruit fly Drosophila toll and belong to the interleukin-1 receptor family [4]. To date, 10 members of the TLR family have been identified in mammals and each TLR recognizes specific PAMP. For example, the lipopolysaccharide of gram negative bacteria is a TLR-4 ligand [5]. One of the central features of this system of microbial recognition is that TLRs activate signaling pathways that are critical for induction of the immune response to the given microbial challenge as periodontal pathology is initiated by gram positive organism and progressed by gram negative pathogen. This study was undertaken to determine the corresponding level of expression of TLR-2 and' TLR-4 in healthy gingiva, gingivitis and chronic periodontitis.
| Materials and methods | | |
Gingival sample were obtained from eight chronic periodontitis and nine gingivitis (3 mild; 3 moderate; 3 severe) patients. Eight control samples were also obtained from healthy individuals who have undergone orthodontic treatement. Gingival tissues were collected at the time of respective surgery from patients. The patients with chronic periodontitis were diagnosed based on the criteria of American Academy of Periodontology classification and they did not suffer any other systemic diseases. All the diseased samples expressed clinical signs of inflammation and were taken from sites with a pocket depth greater than 6mm with evidence of bleeding on probing. The control subjects were systemically and periodontology healthy without gingival inflammation and showed no evidence of bleeding on probing with a pocket depth less than 4mm. All the patients and healthy subjects were nonsmokers from enquiry on general history. These patients had consented to the participation in this study with full knowledge of its content and implications.
The total RNA was isolated from the gingival tissues by single step, acid guanidiun thicyanate phenol chloroform extraction method [6]. The total RNA was transcribed to cDNA using first strand cDNA synthesis kit (Qbiogene, supplied by imperial BioMedics, Chandigarh, India) for RT-PCR according to manufacturer instructions. The TLRs primers were designed fromthe known sequences of TLR-2 and TLR-4 as: TLR-2 5' -GCCAAAGTCTTGATTGATTGG- 3' (sense) and 5'TTGAAGTTCTCCAGCTCCTG-3' (antisense), TLR-4 5'TCCCTCCAGGTTCTTGATTA-3' (sense) and 5'GTAGTGAAGGCAGAGCTGAAA-3' (antisense) which amplifies a 347 and 495 base pair DNA fragment respectively. As a positive control 13-actin designed as 5' AAGGATTCCTATGTGGGC-3' (sense) and 5'- CATCTCTTGCTCGAAGTC-3' (antisense) which were predicted to amplify a 300 base pair DNA fragment. The amplication profile was as follows: denaturing at 94°C for 1 min; annealing at optimal temperature for TLR-2, TLR-4 and 13-actin gene from control as the control. The relative expression of each TLR-2 and TLR-4 gene from control, gingivitis and chronic periodontitis tissues were compared. The differences in the levels of expression of TLR-2 and TLR4 from control, gingivitis and chronic periodontitis tissues were analyzed using t-test for comparison between groups and ANOVAfor comparison within groups.
| Results and discussion | | |
The results showed that both the TLRs were expressed in control and the expression of TLR-2 was increased compared to TLR-4 (not significant). The expression of TLR-2 and TLR-4 was significantly elevated in tissues of gingivitis and chronic periodontitis compared to control [Figure - 1]. In gingivitis, TLR-2 expression was increased compared to TLR-4 (P<0.01). The expression of TLR-4 was significantly increased in chronic periodontitis compared to TLR-2 [Figure - 2]. The discovery of mammalian TLRs has provided new insight into mechanism of inmate immunity to microbial pathogens. Activation of TLRs
leads to the induction of antimicrobial pathways central to irmate defense as well as the up regulation of antigen presentation molecules and secretion of cytokines that influence the nature of adaptive immune response [7].The periodontium is integrally composed of the alveolar bone. Periodontal disease is initiated by microbial colonization of the superficially placed gingiva leading to inflammation of this tissue. This initial colonization is of a gram positive nature which later by means of microbial succession turns into a gram negative flora. The deeper structures like the periodontal ligament getting inflamed in untreated conditions with the predominance of gram negative is an ideal situation to study the amount of expression of TLR-2 and TLR-4.
TLR-2 and TLR-4 were found to be expressed in healthy human gingival tissues [8].The bacteria associated with periodontal health are primarily gram positive facultative species and small proportions of gram negative species are also found [9]. Studies have shown that human gingival fibroblasts expressed TLR-2 and TLR-4, which turned out to be significantly elevated in inflammation [10]. In our study, TLR-2 was expressed more in control than TLR-4, but the increase was not statistically significant.
As expected, we found a significant increase in TLR-2 expression in gingivitis as compared to control. The microbiota of gingivitis consists of gram positive rods, gram positive cocci and gram negative cocci [11]. Wang et al found increased expression of TLR-2 in human gingival fibroblasts of inflammatory gingiva than those in healthy group [12]. We observed that the increased expression of TLR-2 was statistically significant compared to TLR-4 in gingivitis and we also found more expression of TLR-2 in severe gingivitis tissues compared to mild and moderate gingivitis tissue samples. Gingival epithelial cells are central components of the barrier between oral micro flora and internal tissue. Human gingival epithelial cells predominantly expressed TLR-2 but not TLR-4 [13]. Contrary to our findings, Mori et al investigated the expression of TLR-2 and TLR-4 in human periodontal disease and showed higher TLR-2 positive cells in mild group and higher TLR-4 positive cells in severe gingivitis [14]. The bacteria found in severe gingivitis consist of roughly equal proportion of gram-positive (56%) and gram-negative (44%) species [15]. Though gram-negative bacteria were present in severe gingivitis, grain-positive bacteria were also found, confirming the increased expression of TLR-2 in severe gingivitis.
Interestingly, in periodontitis, TLR-4 was significantly more expressed than TLR-2. The structure of sub gingival plaque in periodontitis consists of, dense layer of gram positive organisms between this layer and pocket epithelium; spirochetes and other motile forms at the base of the pocket [16]. It is presently accepted that periodontal disease is initiated and perpetuated by specific gram negative bacteria, among which the black pigmented anaerobeP gingivalis has been implicated as the putative pathogen of periodontal disease. P gingivalis LPS has been considered to be an important pathogenic component in the initiation and development of periodontal disease, because bacterial LPS are known to be a potent stimulator of inflammatory cytokine production and bone resorption [17]. Human gingiva is exposed to a high density and diversity of gram positive and gram negative bacteria It is infiltrated by large number of TLR-2 and TLR-4 positve cells and that their numbers increase significantly in chronic periodontitis, relative to health [18].
TLR-4 is the dominant receptor for LPS, whereas TLR-2 is not required for LP S recognition [19]. TLR-2 mediates signals from other bacterial components including lipoteichoic acid, peptidoglycan and lipoprotein/ lipopoptides [20]. TLR-2 was significantly increased in chronic periodontitis compared to gingivitis. Bacteroids forsythus is a gram negative, anaerobic, fusiform bacterium and is considered to be an etiological agent in periodontal disease. It was found that signaling by B forsythus lipoprotein was mediated by TLR-2 but not TLR-4 [21]. In addition, TLR-2 participates, at least partly, in the signaling pathway to induce chemokine production against Pgingivalis components, probably other than LPS [22]. Studies have shown that human gingival fibroblasts expressed TLR-4 constitutively and that stimulation with P gingivalis LPS increased their levels of expression [23]. Hatakeyama et al reported that human gingival fibroblasts and human periodontal ligament fibroblasts expressed TLR-2 more strongly than human gingival fibroblasts [8]. From these findings, it was concluded that TLR-2 and' TLR-4 on gingival tissues recognize different bacterial cell wall component. So this pilot study of TLR-2 and TLR-4 expression in gingivitis and chronic periodontitis pave way for future studies on changes in the ratio of TLR-2 to TLR-4 in different stages gingivitis and periodontitis.
| References | | |
| 1. | Haffajee AD and Socransky SS: Microbial etiological agents of destructive periodontal disease, Periodonto12000, 5: 78-111,1994.  |
| 2. | Moore WEC and Moore LVH: The bacteria of periodontal diseases, Periodontology 2000, 5: 6677,1994. |
| 3. | TakedaK,KaishoTandAkiraS:Toll-likereceptors, Anna Rev hnmunol, 21: 335-376, 2003. |
| 4. | O'Neill LA: Signal transduction pathways activated by the IL - 1 receptor/toll-like receptor superfamily Corr Top Microbiol Immunol, 270:47-61, 2002. |
| 5. | Lemaitre B, Nicolas E, Michut L, Reichhart JM and Hoffman JA: The Dorsoventral regulatory gene cassette spatzel/Toll/cactus controls the potent antifungal response in drosophila adults, Cell, 86: 973-983,1996. |
| 6. | Chomezynski P and Sacchi N: RNA isolation by single step of acid guanidium thiocyanate- phenolchloroform extraction, Ann Biochem, 163-2: 156159,1987. |
| 7. | Janeway Jr CA and Medzhitov R: hmate immune recognition,Amm Rev Immunol, 20: 197-216,2002. |
| 8. | Hatakeyanmra J, Tamai R and Sugiyama S: Contrasting responses of human gingival and periodontal ligament fibroblasts to bacterial cell surface components through CD14/Toll-like receptor system oral Microbiol hrrmunol, 18: 1423,2003. |
| 9. | Socransky SS and Haffajee AD: The bacterial etiology of destruction disease: Current concepts, J Periodontol, 63; 322,1992. |
| 10. | Uehara A, Sugawara S and Tahada H: Priming of human oral epithelial cells by interferon gamma to secrete cytokines in response to lipopoly saccharides, lipoteichoic acids and peptidolycans, J Med Microbiol, 51: 626-634,2002. |
| 11. | Theilade E, Wright Wh, Jensen SB and Leo H: Experimental gingivitis in man It. A longitudinal clinical and bacteriological investigation, J PeriodontolRes,1:1,1966. |
| 12. | Wang PL, Ohma K, Flrjii T, Oido-Mori M, Kowashi Y; Kikuchi M and et al : DNAmicro array analysis of human gingival fibroblasts from healthy and inflammatory gingival tissues, Biochem Biophys Res Common, 305: 970-973, 2003. |
| 13. | Asai Y, Ohyama Y, Gen K and Ogawa T: Bacterial fimbriae and their peptides active human gingival epithlial cells through TLR-2, Infect Immun, 69: 7387-7395,2001. |
| 14. | MoriY,YoshimuraA,UkaiT.Lien E.EspevikTand HaraY: hnmunohistochemical localization of Tolllike receptor 2 and 4 in gingival tissue from patients with peridontitis oral Microbiol Inmrunol, 18: 5458, 2003. |
| 15. | Slot J: Subgingival microflora and periodontal disease, J Clin Periodontol, 6: 35 |
| 16. | Hamada S, Fujiwara T and Maihara J: Bacterial endotoxic substances and their effects on host cells. In: Molecular pathogenesis of periodontal disease. Genco R, I-Iamada S, Lehner J, McGhee J, Mergenhagen S, (Eds), Washington DC: ASM Press. pages 105-117,1994. |
| 17. | Muthukura M, Jotnani R and cutler CW: Oral muscosal endotoxin tolerance induction in chronic periodontitis, Infect human, 73; 387-694, 2005. |
| 18. | Brightbill HD, Libraty DH, Krutzik SR, Yang RB, Belisle JT, Bleharski JR and et al : Host defense mechanisms triggered by microbial lipoproteins through toll-like receptors, Science, 285: 732-736, 1999. |
| 19. | Schwandner R, Dziarski R, WescheH, RotheM and Kirsching CJ: Peptidoglycan and lipoteichioc acid induced cell activation mediated by toll-like receptor 2,JBiolChem,274:17406-17406,1999. |
| 20. | Alexopoulou L, Thomas V, Schnsre M, Lobet Y, Anguit J, Schoen RT and et al : Hyporesponsivenss to vaccination with Borrelia burgdorferi OspA in humana and in TLR-1 and TLR-2 deficient mice, NatMed, 8:878-884,2002. |
| 21. | Hasebe A, Yoshimura S, Into T, Kataoka H, Tanaka S, Arakawa S and et al : Biological activities of Bacteroides forsythus lipoproteins and their possible pathological roles in periodontal disease, Infechrrmun,72:1318-1325,2004. |
| 22. | Kusumoto Y, Hirano H, Saitoh K, Yamada S, Takedachi M, Nazaki T, et al : Human gingival epithelial cell produce chemotactic factors IL-8 and monocyte chemoattactant protein-1 after stimulation with Porphyromonas gingivalis via Toll-like receptor-2, J Periodontol, 75: 370-379, 2004. |
| 23. | Tabeta K, Yamazaki K, Akashi S, Miyake K, KumadaH. Umemoto T and et al : Toll like receptos confer responsiveness to lipopolysaccharide, from Phorphyromonas gingivalis in human gingival fibroblast, Infect fibroblast, Infect human, 68: 3731-3735,2000. |
Correspondence Address:
S M Sarah
Department of Periodontics, Sri Ramachandra Medical College & Research Institute, Porur, Chenai
India
 Source of Support: None, Conflict of Interest: None  | Check |
DOI: 10.4103/0970-9290.29879
Figures
[Figure - 1], [Figure - 2] |
|
| This article has been cited by | | 1 |
Molecular Pathogenesis of Human Immunodeficiency Virus-Associated Disease of Oropharyngeal Mucosal Epithelium |
|
| Sharof M. Tugizov | | Biomedicines. 2023; 11(5): 1444 | | [Pubmed] | [DOI] | | | 2 |
Wnt Signaling Activation in Gingival Epithelial Cells and Macrophages of Experimental Periodontitis |
|
| Ying Chen, Yang Hu | | Dentistry Journal. 2023; 11(5): 129 | | [Pubmed] | [DOI] | | | 3 |
Immunological study of orthodontically treated patients recovering from COVID-19 in Babylon Province, Iraq |
|
| BasmaAbdel Khaleq Eidan, ThaerJaber Al-Khafaji, AhmedMohammed Abbas | | Medical Journal of Babylon. 2023; 20(2): 283 | | [Pubmed] | [DOI] | | | 4 |
Toll-like Receptors: Molecular Microbe Sensors in Periodontium |
|
| Alluri Siddhartha Varma, Girish Suragimath, Apurva Pisal, Pooja R Disale, Sameer Zope | | World Journal of Dentistry. 2019; 10(5): 396 | | [Pubmed] | [DOI] | | | 5 |
Activation of local innate immune signal induces periodontitis in microbiota-dependent manner |
|
| Nan Wang,Dengsheng Xia | | FEMS Microbiology Letters. 2019; 366(12) | | [Pubmed] | [DOI] | | | 6 |
Activation of local innate immune signal induces periodontitis in microbiota-dependent manner |
|
| Nan Wang,Dengsheng Xia | | FEMS Microbiology Letters. 2019; 366(12) | | [Pubmed] | [DOI] | | | 7 |
Assessment of the involvement of the macrophage migration inhibitory factor-glucocorticoid regulatory dyad in the expression of matrix metalloproteinase-2 during periodontitis |
|
| Josefine Hirschfeld,Mohammed Howait,Alexandru Movila,Marijo Parcina,Isabelle Bekeredjian-Ding,James Deschner,Søren Jepsen,Toshihisa Kawai | | European Journal of Oral Sciences. 2017; 125(5): 345 | | [Pubmed] | [DOI] | | | 8 |
Gingival Toll-like receptor and cytokine messenger RNA levels in equine periodontitis and oral health |
|
| R. Kennedy,D. F. Lappin,P. M. Dixon,D. Bennett,M. P. Riggio | | Equine Veterinary Journal. 2017; 49(3): 294 | | [Pubmed] | [DOI] | | | 9 |
Gingival Toll-like receptor and cytokine messenger RNA levels in equine periodontitis and oral health |
|
| R. Kennedy,D. F. Lappin,P. M. Dixon,D. Bennett,M. P. Riggio | | Equine Veterinary Journal. 2017; 49(3): 294 | | [Pubmed] | [DOI] | | | 10 |
Immunohistochemical localization of TLR2 and CD14 in gingival tissue of healthy individuals and patients with chronic periodontitis |
|
| S Sumedha,VS Kotrashetti,RS Nayak,A Nayak,A Raikar | | Biotechnic & Histochemistry. 2017; 92(7): 487 | | [Pubmed] | [DOI] | | | 11 |
Associations of Toll-Like Receptor and ß-Defensin Polymorphisms with Measures of Periodontal Disease (PD) in HIV+ North American Adults: An Exploratory Study |
|
| Rajeev K. Mehlotra,Noemi B. Hall,Barne Willie,Catherine M. Stein,Aaron Weinberg,Peter A. Zimmerman,Lance T. Vernon,Graham R. Wallace | | PLOS ONE. 2016; 11(10): e0164075 | | [Pubmed] | [DOI] | | | 12 |
Associations of Toll-Like Receptor and ß-Defensin Polymorphisms with Measures of Periodontal Disease (PD) in HIV+ North American Adults: An Exploratory Study |
|
| Rajeev K. Mehlotra,Noemi B. Hall,Barne Willie,Catherine M. Stein,Aaron Weinberg,Peter A. Zimmerman,Lance T. Vernon,Graham R. Wallace | | PLOS ONE. 2016; 11(10): e0164075 | | [Pubmed] | [DOI] | | | 13 |
Prediabetes Enhances Periodontal Inflammation Consistent With Activation of Toll-Like Receptor–Mediated Nuclear Factor-?B Pathway in Rats |
|
| Yanli Huang,Weihua Guo,Jin Zeng,Guoqing Chen,Wenhua Sun,Xuexin Zhang,Weidong Tian | | Journal of Periodontology. 2016; 87(5): e64 | | [Pubmed] | [DOI] | | | 14 |
Prediabetes Enhances Periodontal Inflammation Consistent With Activation of Toll-Like Receptor–Mediated Nuclear Factor-?B Pathway in Rats |
|
| Yanli Huang,Weihua Guo,Jin Zeng,Guoqing Chen,Wenhua Sun,Xuexin Zhang,Weidong Tian | | Journal of Periodontology. 2016; 87(5): e64 | | [Pubmed] | [DOI] | | | 15 |
Effects of High Glucose for Hard Tissue Formation on Type II Diabetes Model Rat Bone Marrow Cells In Vitro |
|
| Makiko Okuda,Yoichiro Taguchi,Saitatsu Takahashi,Akio Tanaka,Makoto Umeda | | Journal of Hard Tissue Biology. 2015; 24(1): 77 | | [Pubmed] | [DOI] | | | 16 |
Effects of High Glucose for Hard Tissue Formation on Type II Diabetes Model Rat Bone Marrow Cells In Vitro |
|
| Makiko Okuda,Yoichiro Taguchi,Saitatsu Takahashi,Akio Tanaka,Makoto Umeda | | Journal of Hard Tissue Biology. 2015; 24(1): 77 | | [Pubmed] | [DOI] | | | 17 |
The role of natural killer cells in periodontitis |
|
| Asaf Wilensky,Stella Chaushu,Lior Shapira | | Periodontology 2000. 2015; 69(1): 128 | | [Pubmed] | [DOI] | | | 18 |
Expression markers of innate and adaptive immunity in gingival biopsies of patients with chronic generalized periodontitis during treatment |
|
| E. Sh. Grigorovich,R. V. Gorodilov,K. I. Arsent’eva | | Stomatologiya. 2015; 94(5): 17 | | [Pubmed] | [DOI] | | | 19 |
Expression markers of innate and adaptive immunity in gingival biopsies of patients with chronic generalized periodontitis during treatment |
|
| E. Sh. Grigorovich,R. V. Gorodilov,K. I. Arsent’eva | | Stomatologiya. 2015; 94(5): 17 | | [Pubmed] | [DOI] | | | 20 |
Cellular crosstalk mechanism of Toll-like receptors in gingival overgrowth (Review) |
|
| TAMILSELVAN SUBRAMANI,VIDHYA RATHNAVELU,NOORJAHAN BANU ALITHEEN,PARASURAMAN PADMANABHAN | | International Journal of Molecular Medicine. 2015; 35(5): 1151 | | [Pubmed] | [DOI] | | | 21 |
Toll-Like Receptor 4 Mediated Hyper-Responsiveness of Gingival Epithelial Cells to LPS in High-Glucose Environment |
|
| Xi Yang,Jincai Zhang,Jia Ni,Bin Ouyang,Dan Wang,Shigao Luo,Baoyi Xie,Dongying Xuan | | Journal of Periodontology. 2014; : 1 | | [Pubmed] | [DOI] | | | 22 |
Correlation of TLR-4, IL-18, Transaminases and Uric Acid in the Patients With Chronic Periodontitis and Healthy Adults |
|
| Shaheena Banu,Nasimudeen R. Jabir,Nanjappa C. Manjunath,Mohammad Amjad Kamal,Kopparam Rajendra Vinod Kumar,Rekha Mohan,Syed Kashif Zaidi,Mohd Shahnawaz Khan,Shams Tabrez | | Journal of Periodontology. 2014; : 1 | | [Pubmed] | [DOI] | | | 23 |
High Mobility Group Box1 (HMGB1) released from cancer cells induces the expression of pro-inflammatory cytokines in peritoneal fibroblasts |
|
| Anna Abe,Takeshi Kuwata,Chisako Yamauchi,Youichi Higuchi,Atsushi Ochiai | | Pathology International. 2014; 64(6): 267 | | [Pubmed] | [DOI] | | | 24 |
Adhesion of monocyte to periodontal fibroblast requires activation of NOD1/2- and TLR4-mediated LFA-1 and VLA-4 |
|
| Nitin JianruLiu,Wenyi Liu,Ying Xie,Yixiang Wang,Xiangying Ouyang | | Archives of Oral Biology. 2014; | | [Pubmed] | [DOI] | | | 25 |
Comparison of relative TLR-2 and TLR-4 expression level of disease and healthy gingival tissue of smoking and non-smoking patients and periodontally healthy control patients |
|
| K Fatemi,M Radvar,A Rezaee,H Rafatpanah,H Azangoo khiavi,Y Dadpour,N Radvar | | Australian Dental Journal. 2013; 58(3): 315 | | [Pubmed] | [DOI] | | | 26 |
The role of Toll-like receptor 2 and 4 in gingival tissues of chronic periodontitis subjects with type 2 diabetes |
|
| A. Promsudthi,S. Poomsawat,W. Limsricharoen | | Journal of Periodontal Research. 2013; : n/a | | [Pubmed] | [DOI] | | | 27 |
Expression of Immune-Inflammatory Markers in Sites of Chronic Periodontitis in Patients With Type 2 Diabetes |
|
| Poliana Mendes Duarte, Tamires Szeremeske Miranda, Jadson Almeida Lima, Tiago Eduardo Dias Gonçalves, Vanessa Renata Santos, Marta Ferreira Bastos, Fernanda Vieira Ribeiro | | Journal of Periodontology. 2012; 83(4): 426 | | [VIEW] | [DOI] | | | 28 |
Expression of toll-like receptors 2, 4 and 9 is increased in gingival tissue from patients with type 2 diabetes and chronic periodontitis |
|
| N. R. Rojo-Botello,A. L. García-Hernández,L. Moreno-Fierros | | Journal of Periodontal Research. 2012; 47(1): 62 | | [Pubmed] | [DOI] | | | 29 |
A preliminary study on the FAM5C expression in generalized chronic periodontitis |
|
| FV Ribeiro,VR Santos,MF Bastos,TS de Miranda,AR Vieira,LC de Figueiredo,PM Duarte | | Oral Diseases. 2012; 18(2): 147 | | [Pubmed] | [DOI] | | | 30 |
Bradykinin promotes Toll like receptor-4 expression in human gingival fibroblasts |
|
| Gloria Gutiérrez-Venegas,Juan Antonio Arreguín-Cano,Cristina Hernández-Bermúdez | | International Immunopharmacology. 2012; 14(4): 538 | | [Pubmed] | [DOI] | | | 31 |
Bradykinin promotes Toll like receptor-4 expression in human gingival fibroblasts |
|
| Gutiérrez-Venegas, G. and ArreguÃn-Cano, J.A. and Hernández-Bermúdez, C. | | International Immunopharmacology. 2012; 14(4): 538-545 | | [Pubmed] | | | 32 |
A preliminary study on the FAM5C expression in generalized chronic periodontitis |
|
| Ribeiro, F.V. and Santos, V.R. and Bastos, M.F. and de Miranda, T.S. and Vieira, A.R. and de Figueiredo, L.C. and Duarte, P.M. | | Oral Diseases. 2012; 18(2): 147-152 | | [Pubmed] | | | 33 |
Expression of toll-like receptors 2, 4 and 9 is increased in gingival tissue from patients with type 2 diabetes and chronic periodontitis |
|
| Rojo-Botello, N.R. and GarcÃa-Hernández, A.L. and Moreno-Fierros, L. | | Journal of Periodontal Research. 2012; 47(1): 62-73 | | [Pubmed] | | | 34 |
High glucose concentrations alter the biomineralization process in human osteoblastic cells |
|
| A. García-Hernández, H. Arzate, I. Gil-Chavarría, R. Rojo, L. Moreno-Fierros | | Bone. 2011; | | [VIEW] | [DOI] | | | 35 |
Toll like receptor 4 and membrane-bound CD14 expressions in gingivitis, periodontitis and CsA-induced gingival overgrowth |
|
| Sema Becerik, Nazan Özsan, Ali Gürkan, Veli Özgen Öztürk, Gül Atilla, Gülnur Emingil | | Archives of Oral Biology. 2011; 56(5): 456 | | [VIEW] | [DOI] | | | 36 |
Expression of Immune-Inflammatory Markers in Sites of Chronic Periodontitis in Type 2 Diabetic Subjects |
|
| Poliana Mendes Duarte, Tamires Szeremeske de Miranda, Jadson Almeida Lima, Tiago Eduardo Dias Gonçalves, Vanessa Renata Santos, Marta Ferreira Bastos, Fernanda Vieira Ribeiro | | Journal of Periodontology. 2011; : 1 | | [VIEW] | [DOI] | | | 37 |
Variability in Toll-like Receptor Genes and Their Relation to Occurrence of Periodontal Pathogens in Chronic Periodontitis |
|
| L. Hollá, B. Hrdlicková, J. Vokurka, P. Augustín, A. Fassmann, J. Vanek | | Ceská stomatologie/Praktické zubní lékarství. 2011; 111(5): 107 | | [Pubmed] | [DOI] | | | 38 |
Association of Toll-like receptor 9 haplotypes with chronic periodontitis in Czech population |
|
| Lydie Izakovicova Holla, Jan Vokurka, Barbara Hrdlickova, Peter Augustin, Antonin Fassmann | | Journal Of Clinical Periodontology. 2010; 37(2): 152-159 | | [Pubmed] | [DOI] | | | 39 |
TLR4 and IL-18 gene variants in chronic periodontitis: Impact on disease susceptibility and severity |
|
| Noack, B., Grgens, H., Lorenz, K., Schackert, H.K., Hoffmann, T. | | Immunological Investigations. 2009; 38(3-4): 297-310 | | [Pubmed] | | | 40 |
The role of toll-like receptors in pathogenesis of periodontitis [Znaczenie Toll-podobnych receptorów w patogenezie zapaleń przyzebia] |
|
| Chrzeszczyk, D. and Konopka, T. | | Dental and Medical Problems. 2009; 46(1): 94-103 | | [Pubmed] | | | 41 |
Expressions of TLR-2 and TRL-4 in gingival tissues of patients with periodontitis |
|
| Guo, Q.-M. and Shu, R. | | Journal of Shanghai Jiaotong University (Medical Science). 2009; 29(9): 1045-1048 | | [Pubmed] | | | 42 |
TLR4andIL-18Gene Variants in Chronic Periodontitis: Impact on Disease Susceptibility and Severity |
|
| Barbara Noack,Heike Görgens,Katrin Lorenz,Hans Konrad Schackert,Thomas Hoffmann | | Immunological Investigations. 2009; 38(3-4): 297 | | [Pubmed] | [DOI] | | | 43 |
TLR4andIL-18Gene Variants in Chronic Periodontitis: Impact on Disease Susceptibility and Severity |
|
| Barbara Noack,Heike Görgens,Katrin Lorenz,Hans Konrad Schackert,Thomas Hoffmann | | Immunological Investigations. 2009; 38(3-4): 297 | | [Pubmed] | [DOI] | | | 44 |
Immunohistochemical localization of Toll-like receptors 1-10 in periodontitis |
|
| A. Beklen,M. Hukkanen,R. Richardson,Y. T. Konttinen | | Oral Microbiology and Immunology. 2008; 23(5): 425 | | [Pubmed] | [DOI] | | | 45 |
Immunohistochemical localization of Toll-like receptors 1-10 in periodontitis |
|
| Beklen, A. and Hukkanen, M. and Richardson, R. and Konttinen, Y.T. | | Oral Microbiology and Immunology. 2008; 23(5): 425-431 | | [Pubmed] | |
|
|
|
|
|
|
|
|
|
|
|
|
| Article Access Statistics | | | Viewed | 11550 | | | Printed | 586 | | | Emailed | 5 | | | PDF Downloaded | 738 | | | Comments | [Add] | | | Cited by others | 45 | | |
|
|
Users online:
