• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of iaiPermissionsJournals.ASM.orgJournalIAI ArticleJournal InfoAuthorsReviewers
Infect Immun. Jul 1996; 64(7): 2371–2380.
PMCID: PMC174085

Bacterially induced bone destruction: mechanisms and misconceptions.


Normal bone remodelling requires the coordinated regulation of the genesis and activity of osteoblast and osteoclast lineages. Any interference with these integrated cellular systems can result in dysregulation of remodelling with the consequent loss of bone matrix. Bacteria are important causes of bone pathology in common conditions such as periodontitis, dental cysts, bacterial arthritis, and osteomyelitis. It is now established that many of the bacteria implicated in bone diseases contain or produce molecules with potent effects on bone cells. Some of these molecules, such as components of the gram-positive cell walls (lipoteichoic acids), are weak stimulators of bone resorption in vitro, while others (PMT, cpn60) are as active as the most active mammalian osteolytic factors such as cytokines like IL-1 and TNF. The complexity of the integration of bone cell lineage development means that there are still question marks over the mechanism of action of many well-known bone-modulatory molecules such as parathyroid hormone. The key questions which must be asked of the now-recognized bacterial bone-modulatory molecules are as follows: (i) what cell population do they bind to, (ii) what is the nature of the receptor and postreceptor events, and (iii) is their action direct or dependent on the induction of secondary extracellular bone-modulating factors such as cytokines, eicosanoids, etc. In the case of LPS, this ubiquitous gram-negative polymer probably binds to osteoblasts or other cells in bone through the CD14 receptor and stimulates them to release cytokines and eicosanoids which then induce the recruitment and activation of osteoclasts. This explains the inhibitor effects of nonsteroidal and anticytokine agents on LPS-induced bone resorption. However, other bacterial factors such as the potent toxin PMT may act by blocking the normal maturation pathway of the osteoblast lineage, thus inducing dysregulation in the tightly regulated process of resorption and replacement of bone matrix. At the present time, it is not possible to define a general mechanism by which bacteria promote loss of bone matrix. Many bacteria are capable of stimulating bone matrix loss, and the information available would suggest that each organism possesses different factors which interact with bone in different ways. With the rapid increase in antibiotic resistance, particularly with Staphylococcus aureus and M. tuberculosis, organisms responsible for much bone pathology in developed countries only two generations ago, we would urge that much greater attention should be focused on the problem of bacterially induced bone remodelling in order to define pathogenetic mechanisms which could be therapeutic targets for the development of new treatment modalities.

Full Text

The Full Text of this article is available as a PDF (302K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Ackermann MR, Adams DA, Gerken LL, Beckman MJ, Rimler RB. Purified Pasteurella multocida protein toxin reduces acid phosphatase-positive osteoclasts in the ventral nasal concha of gnotobiotic pigs. Calcif Tissue Int. 1993 Jun;52(6):455–459. [PubMed]
  • Ackermann MR, Rimler RB, Thurston JR. Experimental model of atrophic rhinitis in gnotobiotic pigs. Infect Immun. 1991 Oct;59(10):3626–3629. [PMC free article] [PubMed]
  • Baker GL, Oddis CV, Medsger TA., Jr Pasteurella multocida polyarticular septic arthritis. J Rheumatol. 1987 Apr;14(2):355–357. [PubMed]
  • Boyce BF, Yoneda T, Lowe C, Soriano P, Mundy GR. Requirement of pp60c-src expression for osteoclasts to form ruffled borders and resorb bone in mice. J Clin Invest. 1992 Oct;90(4):1622–1627. [PMC free article] [PubMed]
  • Brandi ML, Hukkanen M, Umeda T, Moradi-Bidhendi N, Bianchi S, Gross SS, Polak JM, MacIntyre I. Bidirectional regulation of osteoclast function by nitric oxide synthase isoforms. Proc Natl Acad Sci U S A. 1995 Mar 28;92(7):2954–2958. [PMC free article] [PubMed]
  • Coates AR, Shinnick TM, Ellis RJ. Chaperonin nomenclature. Mol Microbiol. 1993 May;8(4):787–787. [PubMed]
  • Damoulis PD, Hauschka PV. Cytokines induce nitric oxide production in mouse osteoblasts. Biochem Biophys Res Commun. 1994 Jun 15;201(2):924–931. [PubMed]
  • Dewhirst FE. N-acetyl muramyl dipeptide stimulation of bone resorption in tissue culture. Infect Immun. 1982 Jan;35(1):133–137. [PMC free article] [PubMed]
  • Dominick MA, Rimler RB. Turbinate osteoporosis in pigs following intranasal inoculation of purified Pasteurella toxin: histomorphometric and ultrastructural studies. Vet Pathol. 1988 Jan;25(1):17–27. [PubMed]
  • Duncan JR, Ross RF, Switzer WP, Ramsey FK. Pathology of experimental Bordetella bronchiseptica infection in swine: atrophic rhinitis. Am J Vet Res. 1966 Mar;27(117):457–466. [PubMed]
  • Evans RT, Klausen B, Genco RJ. Immunization with fimbrial protein and peptide protects against Porphyromonas gingivalis-induced periodontal tissue destruction. Adv Exp Med Biol. 1992;327:255–262. [PubMed]
  • Felix R, Fleisch H, Frandsen PL. Effect of Pasteurella multocida toxin on bone resorption in vitro. Infect Immun. 1992 Dec;60(12):4984–4988. [PMC free article] [PubMed]
  • Felix R, Hofstetter W, Wetterwald A, Cecchini MG, Fleisch H. Role of colony-stimulating factor-1 in bone metabolism. J Cell Biochem. 1994 Jul;55(3):340–349. [PubMed]
  • Franchi-Miller C, Saffar JL. The 5-lipoxygenase inhibitor BWA4C impairs osteoclastic resorption in a synchronized model of bone remodeling. Bone. 1995 Aug;17(2):185–191. [PubMed]
  • Gallwitz WE, Mundy GR, Lee CH, Qiao M, Roodman GD, Raftery M, Gaskell SJ, Bonewald LF. 5-Lipoxygenase metabolites of arachidonic acid stimulate isolated osteoclasts to resorb calcified matrices. J Biol Chem. 1993 May 15;268(14):10087–10094. [PubMed]
  • Ghoshal NG, Niyo Y. Histomorphologic features of the nasal cavity of pigs exposed to Pasteurella multocida type-D dermonecrotic toxin. Am J Vet Res. 1993 May;54(5):738–742. [PubMed]
  • Girasole G, Jilka RL, Passeri G, Boswell S, Boder G, Williams DC, Manolagas SC. 17 beta-estradiol inhibits interleukin-6 production by bone marrow-derived stromal cells and osteoblasts in vitro: a potential mechanism for the antiosteoporotic effect of estrogens. J Clin Invest. 1992 Mar;89(3):883–891. [PMC free article] [PubMed]
  • Gopalsami C, Yotis W, Corrigan K, Schade S, Keene J, Simonson L. Effect of outer membrane of Treponema denticola on bone resorption. Oral Microbiol Immunol. 1993 Apr;8(2):121–124. [PubMed]
  • Grigoriadis AE, Wang ZQ, Cecchini MG, Hofstetter W, Felix R, Fleisch HA, Wagner EF. c-Fos: a key regulator of osteoclast-macrophage lineage determination and bone remodeling. Science. 1994 Oct 21;266(5184):443–448. [PubMed]
  • Hall TJ, Chambers TJ. Molecular aspects of osteoclast function. Inflamm Res. 1996 Jan;45(1):1–9. [PubMed]
  • Hanazawa S, Amano S, Nakada K, Ohmori Y, Miyoshi T, Hirose K, Kitano S. Biological characterization of interleukin-1-like cytokine produced by cultured bone cells from newborn mouse calvaria. Calcif Tissue Int. 1987 Jul;41(1):31–37. [PubMed]
  • Hanazawa S, Hirose K, Ohmori Y, Amano S, Kitano S. Bacteroides gingivalis fimbriae stimulate production of thymocyte-activating factor by human gingival fibroblasts. Infect Immun. 1988 Jan;56(1):272–274. [PMC free article] [PubMed]
  • Hanazawa S, Kawata Y, Murakami Y, Naganuma K, Amano S, Miyata Y, Kitano S. Porphyromonas gingivalis fimbria-stimulated bone resorption in vitro is inhibited by a tyrosine kinase inhibitor. Infect Immun. 1995 Jun;63(6):2374–2377. [PMC free article] [PubMed]
  • Hanazawa S, Murakami Y, Hirose K, Amano S, Ohmori Y, Higuchi H, Kitano S. Bacteroides (Porphyromonas) gingivalis fimbriae activate mouse peritoneal macrophages and induce gene expression and production of interleukin-1. Infect Immun. 1991 Jun;59(6):1972–1977. [PMC free article] [PubMed]
  • Hanazawa S, Murakami Y, Takeshita A, Kitami H, Ohta K, Amano S, Kitano S. Porphyromonas gingivalis fimbriae induce expression of the neutrophil chemotactic factor KC gene of mouse peritoneal macrophages: role of protein kinase C. Infect Immun. 1992 Apr;60(4):1544–1549. [PMC free article] [PubMed]
  • Hausmann E, Lüderitz O, Knox K, Weinfeld N. Structural requirements for bone resorption by endotoxin and lipoteichoic acid. J Dent Res. 1975 Jun;54(SPEC):B94–B99. [PubMed]
  • Hausmann E, Raisz LG, Miller WA. Endotoxin: stimulation of bone resorption in tissue culture. Science. 1970 May 15;168(3933):862–864. [PubMed]
  • Hausmann E, Weinfeld N, Miller WA. Effects of lipopolysaccharides on bone resorption in tissue culture. Calcif Tissue Res. 1972;9(4):272–282. [PubMed]
  • Helgeland K, Nordby O. Cell cycle-specific growth inhibitory effect on human gingival fibroblasts of a toxin isolated from the culture medium of Actinobacillus actinomycetemcomitans. J Periodontal Res. 1993 May;28(3):161–165. [PubMed]
  • Henderson B, Nair SP, Coates AR. Molecular chaperones and disease. Inflamm Res. 1996 Apr;45(4):155–158. [PubMed]
  • Henderson B, Wilson M. Modulins: a new class of cytokine-inducing, pro-inflammatory bacterial virulence factor. Inflamm Res. 1995 May;44(5):187–197. [PubMed]
  • Henderson B, Wilson M. Cytokine induction by bacteria: beyond lipopolysaccharide. Cytokine. 1996 Apr;8(4):269–282. [PubMed]
  • Higgins TE, Murphy AC, Staddon JM, Lax AJ, Rozengurt E. Pasteurella multocida toxin is a potent inducer of anchorage-independent cell growth. Proc Natl Acad Sci U S A. 1992 May 15;89(10):4240–4244. [PMC free article] [PubMed]
  • Hock JM, Onyia J, Bidwell J. Comparisons of in vivo and in vitro models of the response of osteoblasts to hormonal regulation with aging. Calcif Tissue Int. 1995;56 (Suppl 1):S44–S47. [PubMed]
  • Holt SC, Bramanti TE. Factors in virulence expression and their role in periodontal disease pathogenesis. Crit Rev Oral Biol Med. 1991;2(2):177–281. [PubMed]
  • Horiguchi Y, Nakai T, Kume K. Effects of Bordetella bronchiseptica dermonecrotic toxin on the structure and function of osteoblastic clone MC3T3-e1 cells. Infect Immun. 1991 Mar;59(3):1112–1116. [PMC free article] [PubMed]
  • Horiguchi Y, Sugimoto N, Matsuda M. Stimulation of DNA synthesis in osteoblast-like MC3T3-E1 cells by Bordetella bronchiseptica dermonecrotic toxin. Infect Immun. 1993 Sep;61(9):3611–3615. [PMC free article] [PubMed]
  • Horowitz MC, Coleman DL, Flood PM, Kupper TS, Jilka RL. Parathyroid hormone and lipopolysaccharide induce murine osteoblast-like cells to secrete a cytokine indistinguishable from granulocyte-macrophage colony-stimulating factor. J Clin Invest. 1989 Jan;83(1):149–157. [PMC free article] [PubMed]
  • Iino Y, Hopps RM. The bone-resorbing activities in tissue culture of lipopolysaccharides from the bacteria Actinobacillus actinomycetemcomitans, Bacteroides gingivalis and Capnocytophaga ochracea isolated from human mouths. Arch Oral Biol. 1984;29(1):59–63. [PubMed]
  • Ishihara Y, Nishihara T, Maki E, Noguchi T, Koga T. Role of interleukin-1 and prostaglandin in in vitro bone resorption induced by Actinobacillus actinomycetemcomitans lipopolysaccharide. J Periodontal Res. 1991 May;26(3 Pt 1):155–160. [PubMed]
  • Ishimi Y, Miyaura C, Jin CH, Akatsu T, Abe E, Nakamura Y, Yamaguchi A, Yoshiki S, Matsuda T, Hirano T, et al. IL-6 is produced by osteoblasts and induces bone resorption. J Immunol. 1990 Nov 15;145(10):3297–3303. [PubMed]
  • Jilka RL, Hangoc G, Girasole G, Passeri G, Williams DC, Abrams JS, Boyce B, Broxmeyer H, Manolagas SC. Increased osteoclast development after estrogen loss: mediation by interleukin-6. Science. 1992 Jul 3;257(5066):88–91. [PubMed]
  • Kamen PR. The effects of bacterial sonicates on human keratinizing stratified squamous epithelium in vitro. J Periodontal Res. 1981 May;16(3):323–330. [PubMed]
  • Kataoka M, Kawamura K, Kondoh T, Wakano Y, Ishida H. Purification of a fibroblast-inhibitory factor from Actinobacillus actinomycetemcomitans Y4. FEMS Microbiol Lett. 1993 Feb 15;107(1):111–114. [PubMed]
  • Kato S, Muro M, Akifusa S, Hanada N, Semba I, Fujii T, Kowashi Y, Nishihara T. Evidence for apoptosis of murine macrophages by Actinobacillus actinomycetemcomitans infection. Infect Immun. 1995 Oct;63(10):3914–3919. [PMC free article] [PubMed]
  • Kawata Y, Hanazawa S, Amano S, Murakami Y, Matsumoto T, Nishida K, Kitano S. Porphyromonas gingivalis fimbriae stimulate bone resorption in vitro. Infect Immun. 1994 Jul;62(7):3012–3016. [PMC free article] [PubMed]
  • Keeting PE, Rifas L, Harris SA, Colvard DS, Spelsberg TC, Peck WA, Riggs BL. Evidence for interleukin-1 beta production by cultured normal human osteoblast-like cells. J Bone Miner Res. 1991 Aug;6(8):827–833. [PubMed]
  • Kimman TG, Löwik CW, van de Wee-Pals LJ, Thesingh CW, Defize P, Kamp EM, Bijvoet OL. Stimulation of bone resorption by inflamed nasal mucosa, dermonecrotic toxin-containing conditioned medium from Pasteurella multocida, and purified dermonecrotic toxin from P. multocida. Infect Immun. 1987 Sep;55(9):2110–2116. [PMC free article] [PubMed]
  • Kirby AC, Meghji S, Nair SP, White P, Reddi K, Nishihara T, Nakashima K, Willis AC, Sim R, Wilson M, et al. The potent bone-resorbing mediator of Actinobacillus actinomycetemcomitans is homologous to the molecular chaperone GroEL. J Clin Invest. 1995 Sep;96(3):1185–1194. [PMC free article] [PubMed]
  • Larjava H, Uitto VJ, Eerola E, Haapasalo M. Inhibition of gingival fibroblast growth by Bacteroides gingivalis. Infect Immun. 1987 Jan;55(1):201–205. [PMC free article] [PubMed]
  • Lensgraf EJ, Greenblatt JJ, Bawden JW. Effect of group A streptococcal peptidoglycan and group A streptococcal cell wall on bone in tissue culture. Arch Oral Biol. 1979;24(7):495–498. [PubMed]
  • Littlewood AJ, Russell J, Harvey GR, Hughes DE, Russell RG, Gowen M. The modulation of the expression of IL-6 and its receptor in human osteoblasts in vitro. Endocrinology. 1991 Sep;129(3):1513–1520. [PubMed]
  • Loomer PM, Ellen RP, Tenenbaum HC. Characterization of inhibitory effects of suspected periodontopathogens on osteogenesis in vitro. Infect Immun. 1995 Sep;63(9):3287–3296. [PMC free article] [PubMed]
  • Loomer PM, Sigusch B, Sukhu B, Ellen RP, Tenenbaum HC. Direct effects of metabolic products and sonicated extracts of Porphyromonas gingivalis 2561 on osteogenesis in vitro. Infect Immun. 1994 Apr;62(4):1289–1297. [PMC free article] [PubMed]
  • Löwik CW, van der Pluijm G, Bloys H, Hoekman K, Bijvoet OL, Aarden LA, Papapoulos SE. Parathyroid hormone (PTH) and PTH-like protein (PLP) stimulate interleukin-6 production by osteogenic cells: a possible role of interleukin-6 in osteoclastogenesis. Biochem Biophys Res Commun. 1989 Aug 15;162(3):1546–1552. [PubMed]
  • Malek R, Fisher JG, Caleca A, Stinson M, van Oss CJ, Lee JY, Cho MI, Genco RJ, Evans RT, Dyer DW. Inactivation of the Porphyromonas gingivalis fimA gene blocks periodontal damage in gnotobiotic rats. J Bacteriol. 1994 Feb;176(4):1052–1059. [PMC free article] [PubMed]
  • Manthey CL, Vogel SN. Interactions of lipopolysaccharide with macrophages. Immunol Ser. 1994;60:63–81. [PubMed]
  • Marie PJ. Human endosteal osteoblastic cells: relationship with bone formation. Calcif Tissue Int. 1995;56 (Suppl 1):S13–S16. [PubMed]
  • Martin TJ, Ng KW. Mechanisms by which cells of the osteoblast lineage control osteoclast formation and activity. J Cell Biochem. 1994 Nov;56(3):357–366. [PubMed]
  • Martineau-Doizé B, Caya I, Gagné S, Jutras I, Dumas G. Effects of Pasteurella multocida toxin on the osteoclast population of the rat. J Comp Pathol. 1993 Jan;108(1):81–91. [PubMed]
  • Martineau-Doizé B, Ménard J, Girard C, Frantz JC, Martineau GP. Effects of purified Pasteurella multocida dermonecrotoxin on the nasal ventral turbinates of fattening pigs: histological observations. Can J Vet Res. 1991 Oct;55(4):377–379. [PMC free article] [PubMed]
  • McMillan RM, Walker ER. Designing therapeutically effective 5-lipoxygenase inhibitors. Trends Pharmacol Sci. 1992 Aug;13(8):323–330. [PubMed]
  • Meghji S, Sandy JR, Scutt AM, Harvey W, Harris M. Stimulation of bone resorption by lipoxygenase metabolites of arachidonic acid. Prostaglandins. 1988 Aug;36(2):139–149. [PubMed]
  • Meghji S, Wilson M, Barber P, Henderson B. Bone resorbing activity of surface-associated material from Actinobacillus actinomycetemcomitans and Eikenella corrodens. J Med Microbiol. 1994 Sep;41(3):197–203. [PubMed]
  • Meghji S, Wilson M, Henderson B, Kinane D. Anti-proliferative and cytotoxic activity of surface-associated material from periodontopathogenic bacteria. Arch Oral Biol. 1992 Aug;37(8):637–644. [PubMed]
  • Meghji S, Henderson B, Nair S, Wilson M. Inhibition of bone DNA and collagen production by surface-associated material from bacteria implicated in the pathology of periodontal disease. J Periodontol. 1992 Sep;63(9):736–742. [PubMed]
  • Meikle MC, Gowen M, Reynolds JJ. Effect of streptococcal cell wall components on bone metabolism in vitro. Calcif Tissue Int. 1982 Jul;34(4):350–364. [PubMed]
  • Mihara J, Miyazawa Y, Holt SC. Modulation of growth and function of human gingival fibroblasts by fibroblast-activating factor derived from Porphyromonas gingivalis W50. Infect Immun. 1993 Feb;61(2):596–601. [PMC free article] [PubMed]
  • Mihara J, Yoneda T, Holt SC. Role of Porphyromonas gingivalis-derived fibroblast-activating factor in bone resorption. Infect Immun. 1993 Aug;61(8):3562–3564. [PMC free article] [PubMed]
  • Millar SJ, Goldstein EG, Levine MJ, Hausmann E. Modulation of bone metabolism by two chemically distinct lipopolysaccharide fractions from Bacteroides gingivalis. Infect Immun. 1986 Jan;51(1):302–306. [PMC free article] [PubMed]
  • Moncada S, Higgs A. The L-arginine-nitric oxide pathway. N Engl J Med. 1993 Dec 30;329(27):2002–2012. [PubMed]
  • Mota GF, Carneiro CR, Gomes L, Lopes JD. Monoclonal antibodies to Staphylococcus aureus laminin-binding proteins cross-react with mammalian cells. Infect Immun. 1988 Jun;56(6):1580–1584. [PMC free article] [PubMed]
  • Mullan PB, Lax AJ. Pasteurella multocida toxin is a mitogen for bone cells in primary culture. Infect Immun. 1996 Mar;64(3):959–965. [PMC free article] [PubMed]
  • Nair S, Song Y, Meghji S, Reddi K, Harris M, Ross A, Poole S, Wilson M, Henderson B. Surface-associated proteins from Staphylococcus aureus demonstrate potent bone resorbing activity. J Bone Miner Res. 1995 May;10(5):726–734. [PubMed]
  • Nishihara T, Ohsaki Y, Ueda N, Saito N, Mundy GR. Mouse interleukin-1 receptor antagonist induced by Actinobacillus actinomycetemcomitans lipopolysaccharide blocks the effects of interleukin-1 on bone resorption and osteoclast-like cell formation. Infect Immun. 1994 Feb;62(2):390–397. [PMC free article] [PubMed]
  • Nishihara T, Ueda N, Amano K, Ishihara Y, Hayakawa H, Kuroyanagi T, Ohsaki Y, Nagata K, Noguchi T. Actinobacillus actinomycetemcomitans Y4 capsular-polysaccharide-like polysaccharide promotes osteoclast-like cell formation by interleukin-1 alpha production in mouse marrow cultures. Infect Immun. 1995 May;63(5):1893–1898. [PMC free article] [PubMed]
  • Patti JM, Bremell T, Krajewska-Pietrasik D, Abdelnour A, Tarkowski A, Rydén C, Hök M. The Staphylococcus aureus collagen adhesin is a virulence determinant in experimental septic arthritis. Infect Immun. 1994 Jan;62(1):152–161. [PMC free article] [PubMed]
  • Raisz LG, Alander C, Eilon G, Whitehead SP, Nuki K. Effects of two bacterial products, muramyl dipeptide and endotoxin, on bone resorption in organ culture. Calcif Tissue Int. 1982 Jul;34(4):365–369. [PubMed]
  • Raisz LG, Nuki K, Alander CB, Craig RG. Interactions between bacterial endotoxin and other stimulators of bone resorption in organ culture. J Periodontal Res. 1981 Jan;16(1):1–7. [PubMed]
  • Raja RH, Raucci G, Hook M. Peptide analogs to a fibronectin receptor inhibit attachment of Staphylococcus aureus to fibronectin-containing substrates. Infect Immun. 1990 Aug;58(8):2593–2598. [PMC free article] [PubMed]
  • Ralston SH, Ho LP, Helfrich MH, Grabowski PS, Johnston PW, Benjamin N. Nitric oxide: a cytokine-induced regulator of bone resorption. J Bone Miner Res. 1995 Jul;10(7):1040–1049. [PubMed]
  • Reddi K, Meghji S, Wilson M, Henderson B. Comparison of the osteolytic activity of surface-associated proteins of bacteria implicated in periodontal disease. Oral Dis. 1995 Mar;1(1):26–31. [PubMed]
  • Reddi K, Poole S, Nair S, Meghji S, Henderson B, Wilson M. Lipid A-associated proteins from periodontopathogenic bacteria induce interleukin-6 production by human gingival fibroblasts and monocytes. FEMS Immunol Med Microbiol. 1995 Apr;11(2):137–144. [PubMed]
  • Retzlaff C, Yamamoto Y, Hoffman PS, Friedman H, Klein TW. Bacterial heat shock proteins directly induce cytokine mRNA and interleukin-1 secretion in macrophage cultures. Infect Immun. 1994 Dec;62(12):5689–5693. [PMC free article] [PubMed]
  • Riancho JA, Salas E, Zarrabeitia MT, Olmos JM, Amado JA, Fernández-Luna JL, González-Macías J. Expression and functional role of nitric oxide synthase in osteoblast-like cells. J Bone Miner Res. 1995 Mar;10(3):439–446. [PubMed]
  • Ross AC. Infected arthroplasties. Curr Opin Rheumatol. 1991 Aug;3(4):628–633. [PubMed]
  • Rutter JM. Atrophic rhinitis in swine. Adv Vet Sci Comp Med. 1985;29:239–279. [PubMed]
  • Rydén C, Yacoub AI, Maxe I, Heinegård D, Oldberg A, Franzén A, Ljungh A, Rubin K. Specific binding of bone sialoprotein to Staphylococcus aureus isolated from patients with osteomyelitis. Eur J Biochem. 1989 Sep 15;184(2):331–336. [PubMed]
  • Saito S, Hayakawa M, Takiguchi H, Abiko Y. Suppression of proliferation of a human B-cell leukaemic cell line derived from acute lymphoblastic leukaemia by soluble factor(s) from Campylobacter rectus. Arch Oral Biol. 1993 Jun;38(6):449–455. [PubMed]
  • Schumann RR, Rietschel ET, Loppnow H. The role of CD14 and lipopolysaccharide-binding protein (LBP) in the activation of different cell types by endotoxin. Med Microbiol Immunol. 1994 Dec;183(6):279–297. [PubMed]
  • Seckinger P, Klein-Nulend J, Alander C, Thompson RC, Dayer JM, Raisz LG. Natural and recombinant human IL-1 receptor antagonists block the effects of IL-1 on bone resorption and prostaglandin production. J Immunol. 1990 Dec 15;145(12):4181–4184. [PubMed]
  • Shenker BJ, Datar S. Fusobacterium nucleatum inhibits human T-cell activation by arresting cells in the mid-G1 phase of the cell cycle. Infect Immun. 1995 Dec;63(12):4830–4836. [PMC free article] [PubMed]
  • Silveira D, Edington N, Smith IM. Ultrastructural changes in the nasal turbinate bones of pigs in early infection with Bordetella bronchiseptica. Res Vet Sci. 1982 Jul;33(1):37–42. [PubMed]
  • Sismey-Durrant HJ, Atkinson SJ, Hopps RM, Heath JK. The effect of lipopolysaccharide from bacteroides gingivalis and muramyl dipeptide on osteoblast collagenase release. Calcif Tissue Int. 1989 May;44(5):361–363. [PubMed]
  • Sismey-Durrant HJ, Hopps RM. The effect of lipopolysaccharide from the oral bacterium Bacteroides gingivalis on osteoclastic resorption of sperm-whale dentine slices in vitro. Arch Oral Biol. 1987;32(12):911–913. [PubMed]
  • Smyth MG, Pickersgill RW, Lax AJ. The potent mitogen Pasteurella multocida toxin is highly resistant to proteolysis but becomes susceptible at lysosomal pH. FEBS Lett. 1995 Feb 20;360(1):62–66. [PubMed]
  • Staddon JM, Barker CJ, Murphy AC, Chanter N, Lax AJ, Michell RH, Rozengurt E. Pasteurella multocida toxin, a potent mitogen, increases inositol 1,4,5-trisphosphate and mobilizes Ca2+ in Swiss 3T3 cells. J Biol Chem. 1991 Mar 15;266(8):4840–4847. [PubMed]
  • Stashenko P, Dewhirst FE, Peros WJ, Kent RL, Ago JM. Synergistic interactions between interleukin 1, tumor necrosis factor, and lymphotoxin in bone resorption. J Immunol. 1987 Mar 1;138(5):1464–1468. [PubMed]
  • Sterner-Kock A, Lanske B, Uberschär S, Atkinson MJ. Effects of the Pasteurella multocida toxin on osteoblastic cells in vitro. Vet Pathol. 1995 May;32(3):274–279. [PubMed]
  • Sveen K, Skaug N. Bone resorption stimulated by lipopolysaccharides from Bacteroides, Fusobacterium and Veillonella, and by the lipid A and the polysaccharide part of Fusobacterium lipopolysaccharide. Scand J Dent Res. 1980 Dec;88(6):535–542. [PubMed]
  • Ueda N, Nishihara T, Ishihara Y, Amano K, Kuroyanagi T, Noguchi T. Role of prostaglandin in the formation of osteoclasts induced by capsular-like polysaccharide antigen of Actinobacillus actinomycetemcomitans strain Y4. Oral Microbiol Immunol. 1995 Apr;10(2):69–75. [PubMed]
  • Vaes G. Cellular biology and biochemical mechanism of bone resorption. A review of recent developments on the formation, activation, and mode of action of osteoclasts. Clin Orthop Relat Res. 1988 Jun;(231):239–271. [PubMed]
  • Ward PN, Higgins TE, Murphy AC, Mullan PB, Rozengurt E, Lax AJ. Mutation of a putative ADP-ribosylation motif in the Pasteurella multocida toxin does not affect mitogenic activity. FEBS Lett. 1994 Mar 28;342(1):81–84. [PubMed]
  • White PA, Wilson M, Nair SP, Kirby AC, Reddi K, Henderson B. Characterization of an antiproliferative surface-associated protein from Actinobacillus actinomycetemcomitans which can be neutralized by sera from a proportion of patients with localized juvenile periodontitis. Infect Immun. 1995 Jul;63(7):2612–2618. [PMC free article] [PubMed]
  • Wilson M. Biological activities of lipopolysaccharides from oral bacteria and their relevance to the pathogenesis of chronic periodontitis. Sci Prog. 1995;78(Pt 1):19–34. [PubMed]
  • Wilson M, Henderson B. Virulence factors of Actinobacillus actinomycetemcomitans relevant to the pathogenesis of inflammatory periodontal diseases. FEMS Microbiol Rev. 1995 Dec;17(4):365–379. [PubMed]
  • Wilson M, Kamin S, Harvey W. Bone resorbing activity of purified capsular material from Actinobacillus actinomycetemcomitans. J Periodontal Res. 1985 Sep;20(5):484–491. [PubMed]
  • Wilson M, Meghji S, Barber P, Henderson B. Biological activities of surface-associated material from Porphyromonas gingivalis. FEMS Immunol Med Microbiol. 1993 Mar;6(2-3):147–155. [PubMed]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)


Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...


Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...