全部 标题 作者
关键词 摘要

OALib Journal期刊
ISSN: 2333-9721
费用:99美元

查看量下载量

相关文章

更多...
PLOS ONE  2014 

Porphyromonas gingivalis GroEL Induces Osteoclastogenesis of Periodontal Ligament Cells and Enhances Alveolar Bone Resorption in Rats

DOI: 10.1371/journal.pone.0102450

Full-Text   Cite this paper   Add to My Lib

Abstract:

Porphyromonas gingivalis is a major periodontal pathogen that contains a variety of virulence factors. The antibody titer to P. gingivalis GroEL, a homologue of HSP60, is significantly higher in periodontitis patients than in healthy control subjects, suggesting that P. gingivalis GroEL is a potential stimulator of periodontal disease. However, the specific role of GroEL in periodontal disease remains unclear. Here, we investigated the effect of P. gingivalis GroEL on human periodontal ligament (PDL) cells in vitro, as well as its effect on alveolar bone resorption in rats in vivo. First, we found that stimulation of PDL cells with recombinant GroEL increased the secretion of the bone resorption-associated cytokines interleukin (IL)-6 and IL-8, potentially via NF-κB activation. Furthermore, GroEL could effectively stimulate PDL cell migration, possibly through activation of integrin α1 and α2 mRNA expression as well as cytoskeletal reorganization. Additionally, GroEL may be involved in osteoclastogenesis via receptor activator of nuclear factor κ-B ligand (RANKL) activation and alkaline phosphatase (ALP) mRNA inhibition in PDL cells. Finally, we inoculated GroEL into rat gingiva, and the results of microcomputed tomography (micro-CT) and histomorphometric assays indicated that the administration of GroEL significantly increased inflammation and bone loss. In conclusion, P. gingivalis GroEL may act as a potent virulence factor, contributing to osteoclastogenesis of PDL cells and resulting in periodontal disease with alveolar bone resorption.

References

[1]  Ezzo PJ, Cutler CW (2003) Microorganisms as risk indicators for periodontal disease. Periodontol 2000 32: 24–35. doi: 10.1046/j.0906-6713.2003.03203.x
[2]  Lamont RJ, Jenkinson HF (2000) Subgingival colonization by Porphyromonas gingivalis. Oral Microbiol Immunol 15: 341–349. doi: 10.1034/j.1399-302x.2000.150601.x
[3]  Malek R, Fisher JG, Caleca A, Stinson M, van Oss CJ, et al. (1994) Inactivation of the Porphyromonas gingivalis fimA gene blocks periodontal damage in gnotobiotic rats. J Bacteriol 176: 1052–1059.
[4]  Reife RA, Shapiro RA, Bamber BA, Berry KK, Mick GE, et al. (1995) Porphyromonas gingivalis lipopolysaccharide is poorly recognized by molecular components of innate host defense in a mouse model of early inflammation. Infect Immun 63: 4686–4694.
[5]  Chung SW, Kang HS, Park HR, Kim SJ, Kim SJ, et al. (2003) Immune responses to heat shock protein in Porphyromonas gingivalis-infected periodontitis and atherosclerosis patients. J Periodontal Res 38: 388–393. doi: 10.1034/j.1600-0765.2003.00664.x
[6]  Tabeta K, Yamazaki K, Hotokezaka H, Yoshie H, Hara K (2000) Elevated humoral immune response to heat shock protein 60 (hsp60) family in periodontitis patients. Clin Exp Immunol 120: 285–293. doi: 10.1046/j.1365-2249.2000.01216.x
[7]  Yamazaki K, Ueki-Maruayama K, Honda T, Nakajima T, Seymour GJ (2004) Effect of periodontal treatment on the serum antibody levels to heat shock proteins. Clin Exp Immunol 135: 478–482. doi: 10.1111/j.1365-2249.2003.02375.x
[8]  Fukui M, Hinode D, Yokoyama M, Tanabe S, Yoshioka M (2006) Salivary immunoglobulin A directed to oral microbial GroEL in patients with periodontitis and their potential protective role. Oral Microbiol Immunol 21: 289–295. doi: 10.1111/j.1399-302x.2006.00290.x
[9]  Lee JY, Yi NN, Kim US, Choi JS, Kim SJ, et al. (2006) Porphyromonas gingivalis heat shock protein vaccine reduces the alveolar bone loss induced by multiple periodontopathogenic bacteria. J Periodontal Res 41: 10–14. doi: 10.1111/j.1600-0765.2005.00832.x
[10]  Maeda H, Miyamoto M, Kokeguchi S, Kono T, Nishimura F, et al. (2000) Epitope mapping of heat shock protein 60 (GroEL) from Porphyromonas gingivalis. FEMS Immunol Med Microbiol 28: 219–224. doi: 10.1111/j.1574-695x.2000.tb01480.x
[11]  Ueki K, Tabeta K, Yoshie H, Yamazaki K (2002) Self-heat shock protein 60 induces tumour necrosis factor-alpha in monocyte-derived macrophage: possible role in chronic inflammatory periodontal disease. Clin Exp Immunol 127: 72–77. doi: 10.1046/j.1365-2249.2002.01723.x
[12]  Retzlaff C, Yamamoto Y, Hoffman PS, Friedman H, Klein TW (1994) Bacterial heat shock proteins directly induce cytokine mRNA and interleukin-1 secretion in macrophage cultures. Infect Immun 62: 5689–5693.
[13]  Tabona P, Reddi K, Khan S, Nair SP, Crean SJ, et al. (1998) Homogeneous Escherichia coli chaperonin 60 induces IL-1 beta and IL-6 gene expression in human monocytes by a mechanism independent of protein conformation. J Immunol 161: 1414–1421.
[14]  Zhang Y, Doerfler M, Lee TC, Guillemin B, Rom WN (1993) Mechanisms of stimulation of interleukin-1 beta and tumor necrosis factor-alpha by Mycobacterium tuberculosis components. J Clin Invest 91: 2076–2083. doi: 10.1172/jci116430
[15]  Galdiero M, de l’Ero GC, Marcatili A (1997) Cytokine and adhesion molecule expression in human monocytes and endothelial cells stimulated with bacterial heat shock proteins. Infect Immun 65: 699–707.
[16]  Verdegaal ME, Zegveld ST, van Furth R (1996) Heat shock protein 65 induces CD62e, CD106, and CD54 on cultured human endothelial cells and increases their adhesiveness for monocytes and granulocytes. J Immunol 157: 369–376.
[17]  Goulhen F, Hafezi A, Uitto VJ, Hinode D, Nakamura R, et al. (1998) Subcellular localization and cytotoxic activity of the GroEL-like protein isolated from Actinobacillus actinomycetemcomitans. Infect Immun 66: 5307–5313.
[18]  Hinode D, Yoshioka M, Tanabe S, Miki O, Masuda K, et al. (1998) The GroEL-like protein from Campylobacter rectus: immunological characterization and interleukin-6 and -8 induction in human gingival fibroblast. FEMS Microbiol Lett 167: 1–6. doi: 10.1111/j.1574-6968.1998.tb13199.x
[19]  Tanabe S, Hinode D, Yokoyama M, Fukui M, Nakamura R, et al. (2003) Helicobacter pylori and Campylobacter rectus share a common antigen. Oral Microbiol Immunol 18: 79–87. doi: 10.1034/j.1399-302x.2003.00049.x
[20]  Argueta JG, Shiota S, Yamaguchi N, Masuhiro Y, Hanazawa S (2006) Induction of Porphyromonas gingivalis GroEL signaling via binding to Toll-like receptors 2 and 4. Oral Microbiol Immunol 21: 245–251. doi: 10.1111/j.1399-302x.2006.00286.x
[21]  Jonsson D, Wahlin A, Idvall I, Johnsson I, Bratthall G, et al. (2005) Differential effects of estrogen on DNA synthesis in human periodontal ligament and breast cancer cells. J Periodontal Res 40: 401–406. doi: 10.1111/j.1600-0765.2005.00821.x
[22]  Ogata Y, Niisato N, Sakurai T, Furuyama S, Sugiya H (1995) Comparison of the characteristics of human gingival fibroblasts and periodontal ligament cells. J Periodontol 66: 1025–1031. doi: 10.1902/jop.1995.66.12.1025
[23]  Shimabukuro Y, Ichikawa T, Takayama S, Yamada S, Takedachi M, et al. (2005) Fibroblast growth factor-2 regulates the synthesis of hyaluronan by human periodontal ligament cells. J Cell Physiol 203: 557–563. doi: 10.1002/jcp.20256
[24]  Terashima Y, Shimabukuro Y, Terashima H, Ozasa M, Terakura M, et al. (2008) Fibroblast growth factor-2 regulates expression of osteopontin in periodontal ligament cells. J Cell Physiol 216: 640–650. doi: 10.1002/jcp.21443
[25]  Tang S, Morgan KG, Parker C, Ware JA (1997) Requirement for protein kinase C theta for cell cycle progression and formation of actin stress fibers and filopodia in vascular endothelial cells. J Biol Chem 272: 28704–28711. doi: 10.1074/jbc.272.45.28704
[26]  Kanzaki H, Chiba M, Shimizu Y, Mitani H (2001) Dual regulation of osteoclast differentiation by periodontal ligament cells through RANKL stimulation and OPG inhibition. J Dent Res 80: 887–891. doi: 10.1177/00220345010800030801
[27]  Yang YQ, Li XT, Rabie AB, Fu MK, Zhang D (2006) Human periodontal ligament cells express osteoblastic phenotypes under intermittent force loading in vitro. Front Biosci 11: 776–781. doi: 10.2741/1835
[28]  Park CH, Abramson ZR, Taba M Jr, Jin Q, Chang J, et al. (2007) Three-dimensional micro-computed tomographic imaging of alveolar bone in experimental bone loss or repair. J Periodontol 78: 273–281. doi: 10.1902/jop.2007.060252
[29]  Luan Q, Desta T, Chehab L, Sanders VJ, Plattner J, et al. (2008) Inhibition of experimental periodontitis by a topical boron-based antimicrobial. J Dent Res 87: 148–152. doi: 10.1177/154405910808700208
[30]  Katayama I, Li CY, Yam LT (1972) Histochemical study of acid phosphatase isoenzyme in leukemic reticuloendotheliosis. Cancer 29: 157–164. doi: 10.1002/1097-0142(197201)29:1<157::aid-cncr2820290124>3.0.co;2-0
[31]  Hall A (1998) Rho GTPases and the actin cytoskeleton. Science 279: 509–514. doi: 10.1126/science.279.5350.509
[32]  Nakagawa T, Saito A, Hosaka Y, Ishihara K (2003) Gingipains as candidate antigens for Porphyromonas gingivalis vaccine. Keio J Med 52: 158–162. doi: 10.2302/kjm.52.158
[33]  Amano A (2003) Molecular interaction of Porphyromonas gingivalis with host cells: implication for the microbial pathogenesis of periodontal disease. J Periodontol 74: 90–96. doi: 10.1902/jop.2003.74.1.90
[34]  Hiramine H, Watanabe K, Hamada N, Umemoto T (2003) Porphyromonas gingivalis 67-kDa fimbriae induced cytokine production and osteoclast differentiation utilizing TLR2. FEMS Microbiol Lett 229: 49–55. doi: 10.1016/s0378-1097(03)00788-2
[35]  Qi M, Miyakawa H, Kuramitsu HK (2003) Porphyromonas gingivalis induces murine macrophage foam cell formation. Microb Pathog 35: 259–267. doi: 10.1016/j.micpath.2003.07.002
[36]  Vayssier C, Mayrand D, Grenier D (1994) Detection of stress proteins in Porphyromonas gingivalis and other oral bacteria by western immunoblotting analysis. FEMS Microbiol Lett 121: 303–307. doi: 10.1111/j.1574-6968.1994.tb07117.x
[37]  Peetermans WE, Raats CJ, Langermans JA, van Furth R (1994) Mycobacterial heat-shock protein 65 induces proinflammatory cytokines but does not activate human mononuclear phagocytes. Scand J Immunol 39: 613–617. doi: 10.1111/j.1365-3083.1994.tb03421.x
[38]  Lekic P, McCulloch CA (1996) Periodontal ligament cell population: the central role of fibroblasts in creating a unique tissue. Anat Rec 245: 327–341. doi: 10.1002/(sici)1097-0185(199606)245:2<327::aid-ar15>3.0.co;2-r
[39]  Roberts WE, Goodwin WC Jr, Heiner SR (1981) Cellular response to orthodontic force. Dent Clin North Am 25: 3–17.
[40]  Yasuda H, Shima N, Nakagawa N, Yamaguchi K, Kinosaki M, et al. (1998) Osteoclast differentiation factor is a ligand for osteoprotegerin/osteoclastogenesis-inhib?itoryfactor and is identical to TRANCE/RANKL. Proc Natl Acad Sci U S A 95: 3597–3602. doi: 10.1073/pnas.95.7.3597
[41]  Simonet WS, Lacey DL, Dunstan CR, Kelley M, Chang MS, et al. (1997) Osteoprotegerin: a novel secreted protein involved in the regulation of bone density. Cell 89: 309–319. doi: 10.1016/s0092-8674(00)80209-3
[42]  Yasuda H, Shima N, Nakagawa N, Yamaguchi K, Kinosaki M, et al. (1999) A novel molecular mechanism modulating osteoclast differentiation and function. Bone 25: 109–113. doi: 10.1016/s8756-3282(99)00121-0
[43]  Udagawa N, Takahashi N, Jimi E, Matsuzaki K, Tsurukai T, et al. (1999) Osteoblasts/stromal cells stimulate osteoclast activation through expression of osteoclast differentiation factor/RANKL but not macrophage colony-stimulating factor: receptor activator of NF-kappa B ligand. Bone 25: 517–523. doi: 10.1016/s8756-3282(99)00210-0
[44]  Nakashima T, Kobayashi Y, Yamasaki S, Kawakami A, Eguchi K, et al. (2000) Protein expression and functional difference of membrane-bound and soluble receptor activator of NF-kappaB ligand: modulation of the expression by osteotropic factors and cytokines. Biochem Biophys Res Commun 275: 768–775. doi: 10.1006/bbrc.2000.3379
[45]  Belibasakis GN, Bostanci N, Hashim A, Johansson A, Aduse-Opoku J, et al. (2007) Regulation of RANKL and OPG gene expression in human gingival fibroblasts and periodontal ligament cells by Porphyromonas gingivalis: a putative role of the Arg-gingipains. Microb Pathog 43: 46–53. doi: 10.1016/j.micpath.2007.03.001
[46]  Okahashi N, Inaba H, Nakagawa I, Yamamura T, Kuboniwa M, et al. (2004) Porphyromonas gingivalis induces receptor activator of NF-kappaB ligand expression in osteoblasts through the activator protein 1 pathway. Infect Immun 72: 1706–1714. doi: 10.1128/iai.72.3.1706-1714.2004
[47]  Bishop KA, Coy HM, Nerenz RD, Meyer MB, Pike JW (2011) Mouse Rankl expression is regulated in T cells by c-Fos through a cluster of distal regulatory enhancers designated the T cell control region. J Biol Chem 286: 20880–20891. doi: 10.1074/jbc.m111.231548
[48]  Fan X, Roy EM, Murphy TC, Nanes MS, Kim S, et al. (2004) Regulation of RANKL promoter activity is associated with histone remodeling in murine bone stromal cells. J Cell Biochem 93: 807–818. doi: 10.1002/jcb.20217
[49]  Hwang YS, Lee SK, Park KK, Chung WY (2012) Secretion of IL-6 and IL-8 from lysophosphatidic acid-stimulated oral squamous cell carcinoma promotes osteoclastogenesis and bone resorption. Oral Oncol 48: 40–48. doi: 10.1016/j.oraloncology.2011.08.022
[50]  Krajewski AC, Biessei J, Kunze M, Maersch S, Perabo L, et al. (2009) Influence of lipopolysaccharide and interleukin-6 on RANKL and OPG expression and release in human periodontal ligament cells. APMIS 117: 746–754. doi: 10.1111/j.1600-0463.2009.02532.x
[51]  Kirby AC, Meghji S, Nair SP, White P, Reddi K, et al. (1995) The potent bone-resorbing mediator of Actinobacillus actinomycetemcomitans is homologous to the molecular chaperone GroEL. J Clin Invest 96: 1185–1194. doi: 10.1172/jci118150
[52]  Matsushima K, Baldwin ET, Mukaida N (1992) Interleukin-8 and MCAF: novel leukocyte recruitment and activating cytokines. Chem Immunol 51: 236–265. doi: 10.1159/000319090
[53]  Meikle MC (2007) Remodeling the dentofacial skeleton: the biological basis of orthodontics and dentofacial orthopedics. J Dent Res 86: 12–24. doi: 10.1177/154405910708600103
[54]  Bartold PM, Haynes DR (1991) Interleukin-6 production by human gingival fibroblasts. J Periodontal Res 26: 339–345. doi: 10.1111/j.1600-0765.1991.tb02072.x
[55]  Kesavalu L, Chandrasekar B, Ebersole JL (2002) In vivo induction of proinflammatory cytokines in mouse tissue by Porphyromonas gingivalis and Actinobacillus actinomycetemcomitans. Oral Microbiol Immunol 17: 177–180. doi: 10.1034/j.1399-302x.2002.170307.x
[56]  Vicente-Manzanares M, Choi CK, Horwitz AR (2009) Integrins in cell migration–the actin connection. J Cell Sci 122: 199–206. doi: 10.1242/jcs.018564
[57]  Hood JD, Cheresh DA (2002) Role of integrins in cell invasion and migration. Nat Rev Cancer 2: 91–100. doi: 10.1038/nrc727
[58]  Badylak SF (2002) The extracellular matrix as a scaffold for tissue reconstruction. Semin Cell Dev Biol 13: 377–383. doi: 10.1016/s1084952102000940
[59]  Nykvist P, Tu H, Ivaska J, Kapyla J, Pihlajaniemi T, et al. (2000) Distinct recognition of collagen subtypes by alpha(1)beta(1) and alpha(2)beta(1) integrins. Alpha(1)beta(1) mediates cell adhesion to type XIII collagen. J Biol Chem 275: 8255–8261. doi: 10.1074/jbc.275.11.8255
[60]  Knight CG, Morton LF, Peachey AR, Tuckwell DS, Farndale RW, et al. (2000) The collagen-binding A-domains of integrins alpha(1)beta(1) and alpha(2)beta(1) recognize the same specific amino acid sequence, GFOGER, in native (triple-helical) collagens. J Biol Chem 275: 35–40. doi: 10.1074/jbc.275.1.35
[61]  Barczyk M, Carracedo S, Gullberg D (2010) Integrins. Cell Tissue Res 339: 269–280. doi: 10.1007/s00441-009-0834-6
[62]  Lallier TE, Miner QW Jr, Sonnier J, Spencer A (2007) A simple cell motility assay demonstrates differential motility of human periodontal ligament fibroblasts, gingival fibroblasts, and pre-osteoblasts. Cell Tissue Res 328: 339–354. doi: 10.1007/s00441-006-0372-4
[63]  Barczyk MM, Olsen LH, da Franca P, Loos BG, Mustafa K, et al. (2009) A role for alpha11beta1 integrin in the human periodontal ligament. J Dent Res 88: 621–626. doi: 10.1177/0022034509339291

Full-Text

Contact Us

service@oalib.com

QQ:3279437679

WhatsApp +8615387084133