Edema in Oral Mucosa after LPS or Cytokine Exposure

Abstract

Lowering of interstitial fluid pressure (P_if) is an important factor that explains the rapid edema formation in acute inflammation in loose connective tissues. Lipopolysaccharide (LPS) and the pro-inflammatory cytokines interleukin-1beta (IL-1β) and tumor necrosis factor-alpha (TNF-α) are pathogenetic in gingivitis. To test if these substances induce lowering of P_if in rat oral mucosa, we measured P_if with a micropuncture technique. IL-1β and TNF-α caused lowering of P_if, whereas LPS induced an immediate increase in P_if, followed by lowering after 40 min. Measurements of fluid volume distribution showed a significant change in interstitial fluid volume (V_i) 1.5 hr after LPS exposure as V_i changed from 0.41 ± 0.02 to 0.51 ± 0.03 mL/g wet weight (p < 0.05), confirming edema. These findings show that LPS, IL-1β, and TNF-α induce lowering of P_if in the rat oral mucosa and contribute to edema formation in LPS-induced gingivitis.

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References

Attström R, Egelberg J (1970). Emigration of blood neutrophils and monocytes into the gingival crevices. J Periodontal Res 5:48–55.

Berg A, Kirkebo A, Heyeraas KJ (1998). Micropuncture measurements of interstitial fluid pressure in rat nasal mucosa during early inflammatory reactions. J Appl Physiol 85:465–470.

Berg A, Rubin K, Reed RK (2001). Cytochalasin D induces edema formation and lowering of interstitial fluid pressure in rat dermis. Am J Physiol Heart Circ Physiol 281:H7–H13.

Bletsa A, Heyeraas KJ, Haug SR, Berggreen E (2004). IL-1 alpha and TNF-alpha expression in rat periapical lesions and dental pulp after unilateral sympathectomy. Neuroimmunomodulation 11:376–384.

Daffonchio L, Novellini R, Bertuglia S (2002). Protective effect of ketoprofen lysine salt on interleukin-1beta and bradykinin induced inflammatory changes in hamster cheek pouch microcirculation. Inflamm Res 51:223–228.

Del Fabbro M, Francetti L, Bulfamante G, Cribiu M, Miserocchi G, Weinstein RL (2001). Fluid dynamics of gingival tissues in transition from physiological condition to inflammation. J Periodontol 72:65–73.

Fjærtoft M, Johannessen AC, Heyeraas KJ (1992). Micropuncture measurements of interstitial fluid pressure in normal and inflamed gingiva in rats. J Periodontal Res 27:534–538.

Gjerde EA, Eide DM, Brønstad A, Reed R (2004). Problems in physiological experimental animal models investigated with factorial design. J Exp Animal Sci 43:1–12.

Gorska R, Gregorek H, Kowalski J, Laskus-Perendyk A, Syczewska M, Madalinski K (2003). Relationship between clinical parameters and cytokine profiles in inflamed gingival tissue and serum samples from patients with chronic periodontitis. J Clin Periodontol 30:1046–1052.

10.

Gyenge CC, Tenstad O, Wiig H (2003). In vivo determination of steric and electrostatic exclusion of albumin in rat skin and skeletal muscle. J Physiol 552(Pt 3):907–916.

11.

Johannessen AC, Fjærtoft M, Heyeraas KJ (1987). Tissue pressure in rat oral mucosa measured by micropuncture technique. J Periodontal Res 22:139–143.

12.

Koller ME, Reed RK (1992). Increased negativity of interstitial fluid pressure in rat trachea in dextran anaphylaxis. J Appl Physiol 72:53–57.

13.

Lindhe J, Hamp SE, Löe H (1973). Experimental periodontitis in the beagle dog. Int Dent J 23:432–437.

14.

Löe H, Theilade E, Jensen SB, Schiott CR (1967). Experimental gingivitis in man. 3. Influence of antibiotics on gingival plaque development. J Periodontal Res 2:282–289.

15.

Lund T, Wiig H, Reed RK (1988). Acute postburn edema: role of strongly negative interstitial fluid pressure. Am J Physiol 255(5 Pt 2):H1069–H1074.

16.

Miyauchi M, Sato S, Kitagawa S, Hiraoka M, Kudo Y, Ogawa I, et al. (2001). Cytokine expression in rat molar gingival periodontal tissues after topical application of lipopolysaccharide. Histochem Cell Biol 116:57–62.

17.

Nedrebø T, Berg A, Reed RK (1999). Effect of tumor necrosis factor-alpha, IL-1beta, and IL-6 on interstitial fluid pressure in rat skin. Am J Physiol 277(5 Pt 2):H1857–H1862.

18.

Nishida E, Hara Y, Kaneko T, Ikeda Y, Ukai T, Kato I (2001). Bone resorption and local interleukin-1alpha and interleukin-1beta synthesis induced by Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis lipopolysaccharide. J Periodontal Res 36:1–8.

19.

Page RC, Schroeder HE (1976). Pathogenesis of inflammatory periodontal disease. A summary of current work. Lab Invest 34:235–249.

20.

Reed RK, Rubin K, Wiig H, Rodt SA (1992). Blockade of beta 1-integrins in skin causes edema through lowering of interstitial fluid pressure. Circ Res 71:978–983.

21.

Rodt SA, Wiig H, Reed RK (1990). Increased negativity of interstitial fluid pressure contributes to development of oedema in rat skin following application of xylene. Acta Physiol Scand 140:581–586.

22.

Starling EH (1896). On the absorption of fluids from the connective tissue spaces. J Physiol 19:312–326.

23.

Stashenko P, Jandinski JJ, Fujiyoshi P, Rynar J, Socransky SS (1991). Tissue levels of bone resorptive cytokines in periodontal disease. J Periodontol 62:504–509.

24.

Tate RM, Repine JE (1983). Neutrophils and the adult respiratory distress syndrome. Am Rev Respir Dis 128:552–559.

25.

Tingstrom A, Heldin CH, Rubin K (1992). Regulation of fibroblast-mediated collagen gel contraction by platelet-derived growth factor, interleukin-1 alpha and transforming growth factor-beta 1. J Cell Sci 102(Pt 2):315–322.

26.

Uchiba M, Okajima K, Murakami K, Okabe H, Takatsuki K (1995). Endotoxin-induced pulmonary vascular injury is mainly mediated by activated neutrophils in rats. Thromb Res 78:117–125.

27.

Van Dyke TE, Lester MA, Shapira L (1993). The role of the host response in periodontal disease progression: implications for future treatment strategies. J Periodontol 64(8 Suppl):792–806.

28.

Wiederhielm CA, Woodbury JW, Kirk S, Rushmer RF (1964). Pulsatile pressures in the microcirculation of frog’s mesentery. Am J Physiol 207:173–176.

29.

Yoshinari D, Takeyoshi I, Koibuchi Y, Matsumoto K, Kawashima Y, Koyama T, et al. (2001). Effects of a dual inhibitor of tumor necrosis factor-alpha and interleukin-1 on lipopolysaccharide-induced lung injury in rats: involvement of the p38 mitogen-activated protein kinase pathway. Crit Care Med 29:628–634.

30.

Zhu YK, Liu XD, Skold MC, Umino T, Wang H, Romberger DJ, et al. (2001). Cytokine inhibition of fibroblast-induced gel contraction is mediated by PGE(2) and NO acting through separate parallel pathways. Am J Respir Cell Mol Biol 25:245–253.

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