Resolvin D1 protects periodontal ligament

American Journal of Physiology - Cell Physiology

Volumn 305, Issue 6, 2013, Pages

  Mustafa, Manal ^a,b   Zarrough, Ahmed ^b   Bolstad, Anne Isine ^c   Lygre, Henning ^c   Mustafa, Kamal ^a   Hasturk, Hatice ^b   Serhan, Charles ^d   Kantarci, Alpdogan ^b   Van Dyke, Thomas E ^b  

^a UNIVERSITY OF BERGEN   (Norway)

^b FORSYTH INSTITUTE   (United States)

^c UNIVERSITY OF BERGEN   (Norway)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Inflammation; Regeneration; Resolution

Indexed keywords

FIBROBLAST GROWTH FACTOR; INTERLEUKIN 1BETA; LEUKOTRIENE B4; LIPID; LIPOXIN A; PROSTAGLANDIN E2; RESOLVIN D1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DENSITY GRADIENT CENTRIFUGATION; FIBROBLAST; HUMAN; HUMAN CELL; HUMAN TISSUE; PERIODONTAL LIGAMENT; PRIORITY JOURNAL; TISSUE REGENERATION; UPREGULATION; WOUND CLOSURE; WOUND HEALING;

INFLAMMATION; REGENERATION; RESOLUTION;

ANTI-INFLAMMATORY AGENTS; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; DINOPROSTONE; DOCOSAHEXAENOIC ACIDS; FIBROBLASTS; HUMANS; INFLAMMATION; INTERLEUKIN-1BETA; LIPOXINS; MONOCYTES; PERIODONTAL LIGAMENT; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION; WOUND HEALING;

EID: 84884384055     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00242.2012     Document Type: Article

References (63)

1. Beertsen W, McCulloch CA, Sodek J. The periodontal ligament: a unique, multifunctional connective tissue. Periodontol 2000 13: 20-40, 1997.
2. Bento AF, Claudino RF, Dutra RC, Marcon R, Calixto JB. Omega-3 fatty acid-derived mediators 17(R)-hydroxy docosahexaenoic acid, aspirin-triggered resolvin D1 and resolvin D2 prevent experimental colitis in mice. J Immunol 187: 1957-1969, 2011.
3. Black SA Jr, Palamakumbura AH, Stan M, Trackman PC. Tissuespecific mechanisms for CCN2/CTGF persistence in fibrotic gingiva: interactions between cAMP and MAPK signaling pathways, and prostaglandin E2-EP3 receptor mediated activation of the c-JUN N-terminal kinase. J Biol Chem 282: 15416-15429, 2007.
4. Bosshardt DD, Sculean A. Does periodontal tissue regeneration really work? Periodontol 2000 51: 208-219, 2009.
5. Campbell EL, Louis NA, Tomassetti SE, Canny GO, Arita M, Serhan CN, Colgan SP. Resolvin E1 promotes mucosal surface clearance of neutrophils: a new paradigm for inflammatory resolution. FASEB J 21: 3162-3170, 2007.
6. Carnes DL, Maeder CL, Graves DT. Cells with osteoblastic phenotypes can be explanted from human gingiva and periodontal ligament. J Periodontol 68: 701-707, 1997.
7. Champagne CM, Buchanan W, Reddy MS, Preisser JS, Beck JD, Offenbacher S. Potential for gingival crevice fluid measures as predictors of risk for periodontal diseases. Periodontol 2000 31: 167-180, 2003.
8. Claria J, Dalli J, Yacoubian S, Gao F, Serhan CN. Resolvin D1 and resolvin D2 govern local inflammatory tone in obese fat. J Immunol 189: 2597-2605, 2012.
9. Crofford LJ, Tan B, McCarthy CJ, Hla T. Involvement of nuclear factor kappa B in the regulation of cyclooxygenase-2 expression by interleukin-1 in rheumatoid synoviocytes. Arthritis Rheum 40: 226-236, 1997.
10. DeWitt DL. Prostaglandin endoperoxide synthase: regulation of enzyme expression. Biochim Biophys Acta 1083: 121-134, 1991.
11. Doggrell SA. Resolvin inflammation with pain. Expert Opin Investig Drugs 19: 1461-1464, 2010.
12. El-Awady AR, Messer RL, Gamal AY, Sharawy MM, Wenger KH, Lapp CA. Periodontal ligament fibroblasts sustain destructive immune modulators of chronic periodontitis. J Periodontol 81: 1324-1335, 2010.
13. Han X, Amar S. Identification of genes differentially expressed in cultured human periodontal ligament fibroblasts vs. human gingival fibroblasts by DNA microarray analysis. J Dent Res 81: 399-405, 2002.
14. Hasturk H, Kantarci A, Goguet-Surmenian E, Blackwood A, Andry C, Serhan CN, Van Dyke TE. Resolvin E1 regulates inflammation at the cellular and tissue level and restores tissue homeostasis in vivo. J Immunol 179: 7021-7029, 2007.
15. Herrera BS, Ohira T, Gao L, Omori K, Yang R, Zhu M, Muscara MN, Serhan CN, Van Dyke TE, Gyurko R. An endogenous regulator of inflammation, resolvin E1, modulates osteoclast differentiation and bone resorption. Br J Pharmacol 155: 1214-1223, 2008.
16. Jakobsson PJ, Thoren S, Morgenstern R, Samuelsson B. Identification of human prostaglandin E synthase: a microsomal, glutathione-dependent, inducible enzyme, constituting a potential novel drug target. Proc Natl Acad Sci USA 96: 7220-7225, 1999.
17. Jonsson D, Nebel D, Bratthall G, Nilsson BO. The human periodontal ligament cell: a fibroblast-like cell acting as an immune cell. J Periodontal Res 46: 153-157, 2011.
18. Kalmar JR, Arnold RR, Warbington ML, Gardner MK. Superior leukocyte separation with a discontinuous one-step Ficoll-Hypaque gradient for the isolation of human neutrophils. J Immunol Methods 110: 275-281, 1988.
19. Kantarci A, Black SA, Xydas CE, Murawel P, Uchida Y, Yucekal-Tuncer B, Atilla G, Emingil G, Uzel MI, Lee A, Firatli E, Sheff M, Hasturk H, Van Dyke TE, Trackman PC. Epithelial and connective tissue cell CTGF/CCN2 expression in gingival fibrosis. J Pathol 210: 59-66, 2006.
20. Kantarci A, Van Dyke TE. Lipoxins in chronic inflammation. Crit Rev Oral Biol Med 14: 4-12, 2003.
21. Kim TH, Kim GD, Jin YH, Park YS, Park CS. Omega-3 fatty acidderived mediator, Resolvin E1, ameliorates 2,4-dinitrofluorobenzene-induced atopic dermatitis in NC/Nga mice. Int Immunopharmacol 14: 384-391, 2012.
22. Kitamura M, Akamatsu M, Machigashira M, Hara Y, Sakagami R, Hirofuji T, Hamachi T, Maeda K, Yokota M, Kido J, Nagata T, Kurihara H, Takashiba S, Sibutani T, Fukuda M, Noguchi T, Yamazaki K, Yoshie H, Ioroi K, Arai T, Nakagawa T, Ito K, Oda S, Izumi Y, Ogata Y, Yamada S, Shimauchi H, Kunimatsu K, Kawanami M, Fujii T, Furuichi Y, Furuuchi T, Sasano T, Imai E, Omae M, Yamada S, Watanuki M, Murakami S. FGF-2 stimulates periodontal regeneration: results of a multi-center randomized clinical trial. J Dent Res 90: 35-40, 2011.
23. Krishnamoorthy S, Recchiuti A, Chiang N, Yacoubian S, Lee CH, Yang R, Petasis NA, Serhan CN. Resolvin D1 binds human phagocytes with evidence for proresolving receptors. Proc Natl Acad Sci USA 107: 1660-1665.
24. Kuru L, Parkar MH, Griffiths GS, Newman HN, Olsen I. Flow cytometry analysis of gingival and periodontal ligament cells. J Dent Res 77: 555-564, 1998.
25. Lallier TE, Spencer A, Fowler MM. Transcript profiling of periodontal fibroblasts and osteoblasts. J Periodontol 76: 1044-1055, 2005.
26. Lekic P, Rojas J, Birek C, Tenenbaum H, McCulloch CA. Phenotypic comparison of periodontal ligament cells in vivo and in vitro. J Periodontal Res 36: 71-79, 2001.
27. Lekic PC, Pender N, McCulloch CA. Is fibroblast heterogeneity relevant to the health, diseases, and treatments of periodontal tissues? Crit Rev Oral Biol Med 8: 253-268, 1997.
28. Levy BD, Clish CB, Schmidt B, Gronert K, Serhan CN. Lipid mediator class switching during acute inflammation: signals in resolution. Nat Immunol 2: 612-619, 2001.
29. Mas E, Croft KD, Zahra P, Barden A, Mori TA. Resolvins D1, D2, and other mediators of self-limited resolution of inflammation in human blood following n-3 fatty acid supplementation. Clin Chem 58: 1476-1484, 2012.
30. McCulloch CA. Origins and functions of cells essential for periodontal repair: the role of fibroblasts in tissue homeostasis. Oral Dis 1: 271-278, 1995.
31. McCulloch CA, Bordin S. Role of fibroblast subpopulations in periodontal physiology and pathology. J Periodontal Res 26: 144-154, 1991.
32. Melcher AH. On the repair potential of periodontal tissues. J Periodontol 47: 256-260, 1976.
33. Morton RS, Dongari-Bagtzoglou AI. Cyclooxygenase-2 is upregulated in inflamed gingival tissues. J Periodontol 72: 461-469, 2001.
34. Murakami S, Takayama S, Ikezawa K, Shimabukuro Y, Kitamura M, Nozaki T, Terashima A, Asano T, Okada H. Regeneration of periodontal tissues by basic fibroblast growth factor. J Periodontal Res 34: 425-430, 1999.
35. Noguchi K, Ruwanpura SM, Yan M, Yoshida N, Ishikawa I. Downregulation of interleukin-1alpha-induced matrix metalloproteinase-13 expression via EP1 receptors by prostaglandin E2 in human periodontal ligament cells. Oral Microbiol Immunol 20: 56-59, 2005.
36. Noguchi K, Shitashige M, Watanabe H, Murota S, Ishikawa I. Interleukin-4 and interferon-gamma inhibit prostaglandin production by interleukin-1beta-stimulated human periodontal ligament fibroblasts. Inflammation 23: 1-13, 1999.
37. Oates TW, Mumford JH, Carnes DL, Cochran DL. Characterization of proliferation and cellular wound fill in periodontal cells using an in vitro wound model. J Periodontol 72: 324-330, 2001.
38. Ohira T, Bannenberg G, Arita M, Takahashi M, Ge Q, Van Dyke TE, Stahl GL, Serhan CN, Badwey JA. A stable aspirin-triggered lipoxin A4 analog blocks phosphorylation of leukocyte-specific protein 1 in human neutrophils. J Immunol 173: 2091-2098, 2004.
39. Page RC. The etiology and pathogenesis of periodontitis. Compend Contin Educ Dent 23: 11-14, 2002.
40. Parkar MH, Kuru L, Giouzeli M, Olsen I. Expression of growth-factor receptors in normal and regenerating human periodontal cells. Arch Oral Biol 46: 275-284, 2001.
41. Pi SH, Lee SK, Hwang YS, Choi MG, Lee SK, Kim EC. Differential expression of periodontal ligament-specific markers and osteogenic differentiation in human papilloma virus 16-immortalized human gingival fibroblasts and periodontal ligament cells. J Periodontal Res 42: 104-113, 2007.
42. Piche JE, Carnes DL Jr, Graves DT. Initial characterization of cells derived from human periodontia. J Dent Res 68: 761-767, 1989.
43. Raisz LG. Physiologic and pathologic roles of prostaglandins and other eicosanoids in bone metabolism. J Nutr 125: 2024S-2027S, 1995.
44. Romanos GE, Schroter-Kermani C, Bernimoulin JP. [Collagen as a basic element of the periodontium: immunohistochemical aspects in the human and animals. 2. Cementum and periodontal ligament]. Parodontology 2: 47-59, 1991.
45. Serhan CN. Lipoxins and aspirin-triggered 15-epi-lipoxins are the first lipid mediators of endogenous anti-inflammation and resolution. Prostaglandins Leukot Essent Fatty Acids 73: 141-162, 2005.
46. Serhan CN. Novel lipid mediators and resolution mechanisms in acute inflammation: to resolve or not? Am J Pathol 177: 1576-1591, 2010.
47. Serhan CN, Chiang N, Van Dyke TE. Resolving inflammation: dual anti-inflammatory and proresolution lipid mediators. Nat Rev Immunol 8: 349-361, 2008.
48. Serhan CN, Hong S, Gronert K, Colgan SP, Devchand PR, Mirick G, Moussignac RL. Resolvins: a family of bioactive products of omega-3 fatty acid transformation circuits initiated by aspirin treatment that counter proinflammation signals. J Exp Med 196: 1025-1037, 2002.
49. Serhan CN, Savill J. Resolution of inflammation: the beginning programs the end. Nat Immunol 6: 1191-1197, 2005.
50. Singer P, Shapiro H, Theilla M, Anbar R, Singer J, Cohen J. Antiinflammatory properties of omega-3 fatty acids in critical illness: novel mechanisms and an integrative perspective. Intensive Care Med 34: 1580-1592, 2008.
51. Sommer C, Birklein F. Resolvins and inflammatory pain. F1000 Med Rep 3: 19, 2011.
52. Spite M, Summers L, Porter TF, Srivastava S, Bhatnagar A, Serhan CN. Resolvin D1 controls inflammation initiated by glutathione-lipid conjugates formed during oxidative stress. Br J Pharmacol 158: 1062-1073, 2009.
53. Stables MJ, Gilroy DW. Old and new generation lipid mediators in acute inflammation and resolution. Prog Lipid Res.
54. Sume SS, Kantarci A, Lee A, Hasturk H, Trackman PC. Epithelial to mesenchymal transition in gingival overgrowth. Am J Pathol 177: 208-218, 2010.
55. Tang Y, Zhang MJ, Hellmann J, Kosuri M, Bhatnagar A, Spite M. Proresolution therapy for the treatment of delayed healing of diabetic wounds. Diabetes 62: 618-627, 2013.
56. Terranova VP, Odziemiec C, Tweden KS, Spadone DP. Repopulation of dentin surfaces by periodontal ligament cells and endothelial cells. Effect of basic fibroblast growth factor. J Periodontol 60: 293-301, 1989.
57. Tipton DA, Gay DC, DeCoster VA. Effect of a cyclooxygenase-2 inhibitor on interleukin-1beta-stimulated activation of the transcription factor nuclear factor-kappa B in human gingival fibroblasts. J Periodontol 78: 542-549, 2007.
58. Trackman PC, Kantarci A. Connective tissue metabolism and gingival overgrowth. Crit Rev Oral Biol Med 15: 165-175, 2004.
59. Vardar S, Buduneli E, Baylas H, Berdeli AH, Buduneli N, Atilla G. Individual and combined effects of selective cyclooxygenase-2 inhibitor and omega-3 fatty acid on endotoxin-induced periodontitis in rats. J Periodontol 76: 99-106, 2005.
60. Wang SB, Hu KM, Seamon KJ, Mani V, Chen Y, Gronert K. Estrogen negatively regulates epithelial wound healing and protective lipid mediator circuits in the cornea. FASEB J 26: 1506-1516, 2012.
61. Wu SH, Chen XQ, Liu B, Wu HJ, Dong L. Efficacy and safety of 15(R/S)-methyl-lipoxin A(4) in topical treatment of infantile eczema. Br J Dermatol 168: 172-178, 2013.
62. Xu ZZ, Ji RR. Resolvins are potent analgesics for arthritic pain. Br J Pharmacol 164: 274-277, 2011.
63. Yucel-Lindberg T, Brunius G, Wondimu B, Anduren I, Modeer T. Enhanced cyclooxygenase-2 mRNA expression in human gingival fibroblasts induced by cell contact with human lymphocytes. Eur J Oral Sci 109: 187-192, 2001.