Beneficial effects of adiponectin on periodontal ligament cells under normal and regenerative conditions

Journal of Diabetes Research

Volumn 2014, Issue , 2014, Pages

  Nokhbehsaim, Marjan ^a   Keser, Sema ^a   Nogueira, Andressa Vilas Boas ^a,b   Cirelli, Joni Augusto ^b   Jepsen, Søren ^a   Jäger, Andreas ^a   Eick, Sigrun ^c   Deschner, James ^a  

^a UNIVERSITY OF BONN   (Germany)

^b SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^c UNIVERSITY OF BERN   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPONECTIN; ADIPONECTIN RECEPTOR 1; ADIPONECTIN RECEPTOR 2; CYCLOOXYGENASE 2; INTERLEUKIN 6; INTERLEUKIN 8; SMAD1 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN; TRANSCRIPTION FACTOR RUNX2; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN; ADIPONECTIN RECEPTOR; ADIPOQ PROTEIN, HUMAN; AUTACOID; MESSENGER RNA; SCLEROPROTEIN; SIGNAL PEPTIDE;

ARTICLE; CELL FUNCTION; CELL PROLIFERATION; CELL REGENERATION; CELLS BY BODY ANATOMY; CONTROLLED STUDY; DRUG EFFICACY; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; IN VITRO STUDY; NONHUMAN; PERIODONTAL LIGAMENT; PERIODONTAL LIGAMENT CELL; PERIODONTICS; PORPHYROMONAS GINGIVALIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGENERATIVE ABILITY; REGENERATIVE MEDICINE; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; UPREGULATION; WOUND HEALING; AGONISTS; CELL CULTURE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PATHOLOGY; REGENERATION; TIME;

ADIPONECTIN; CELL PROLIFERATION; CELLS, CULTURED; EXTRACELLULAR MATRIX PROTEINS; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION MEDIATORS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; PERIODONTAL LIGAMENT; PORPHYROMONAS GINGIVALIS; RECEPTORS, ADIPONECTIN; REGENERATION; RNA, MESSENGER; SIGNAL TRANSDUCTION; TIME FACTORS; WOUND HEALING;

EID: 84910604628     PISSN: 23146745     EISSN: 23146753     Source Type: Journal    
DOI: 10.1155/2014/796565     Document Type: Article

References (84)

1. International Diabetes Federation, IDF Diabetes Atlas, International Diabetes Federation, Brussels, Belgium, 6th edition, 2013.
2. G. A. Stevens, G. M. Singh, Y. Lu, et al., "National, regional, and global trends in adult overweight and obesity prevalences, " Population Health Metrics, vol. 10, article 22, 2012.
3. D. M. Nguyen and H. B. El-Serag, "The epidemiology of obesity, " Gastroenterology Clinics of North America, vol. 39, no. 1, pp. 1-7, 2010.
4. J. Suvan, F. DAiuto, D. R. Moles, A. Petrie, and N. Donos, "Association between overweight/obesity and periodontitis in adults. A systematic review, " Obesity Reviews, vol. 12, no. 501, pp. e381-e404, 2011.
5. B. W. Chaffee and S. J. Weston, "Association between chronic periodontal disease and obesity: a systematic review and metaanalysis, " Journal of Periodontology, vol. 81, no. 12, pp. 1708-1724, 2010.
6. N. G. M. Chvarry, M. V. Vettore, C. Sansone, and A. Sheiham, "The relationship between diabetes mellitus and destructive periodontal disease: a meta-analysis, " Oral Health & Preventive Dentistry, vol. 7, no. 2, pp. 107-127, 2009.
7. Y. S. Khader, A. S. Dauod, S. S. El-Qaderi, A. Alkafajei, and W. Q. Batayha, "Periodontal status of diabetics compared with nondiabetics: a meta-analysis, " Journal of Diabetes and Its Complications, vol. 20, no. 1, pp. 59-68, 2006.
8. B. L. Pihlstrom, B. S. Michalowicz, and N. W. Johnson, "Periodontal diseases, " The Lancet, vol. 366, no. 9499, pp. 1809-1820, 2005.
9. L. Sbordone and C. Bortolaia, "Oral microbial biofilms and plaque-related diseases: microbial communities and their role in the shift from oral health to disease., " Clinical Oral Investigations, vol. 7, no. 4, pp. 181-188, 2003.
10. D. N. Tatakis and P. S. Kumar, "Etiology and pathogenesis of periodontal diseases, " Dental Clinics of North America, vol. 49, no. 3, pp. 491-516, 2005.
11. T. Yucel-Lindberg and T. Båge, "Inflammatory mediators in the pathogenesis of periodontitis, " Expert Reviews in Molecular Medicine, vol. 15, article e7, 22 pages, 2013.
12. L. J. A. Heitz-Mayfield, "How effective is surgical therapy compared with nonsurgical debridement?" Periodontology 2000, vol. 37, no. 1, pp. 72-87, 2005.
13. M. K. McGuire and D. L. Cochran, "Evaluation of human recession defects treated with coronally advanced flaps and either enamel matrix derivative or connective tissue. Part 2: histological evaluation, " Journal of Periodontology, vol. 74, no. 8, pp. 1126-1135, 2003.
14. A. Sculean, R. Alessandri, R. Miron, G. E. Salvi, and D. D. Bosshardt, "Enamel matrix proteins and periodontal wound healing and regeneration, "ClinicalAdvances in Periodontics, vol. 1, pp. 101-117, 2011.
15. R. A. Yukna and J. T. Mellonig, "Histologic evaluation of periodontal healing in humans following regenerative therapy with enamel matrix derivative. A 10-case series, " Journal of Periodontology, vol. 71, no. 5, pp. 752-759, 2000.
16. D. D. Bosshardt, "Biological mediators and periodontal regeneration: a review of enamel matrix proteins at the cellular and molecular levels, " Journal of Clinical Periodontology, vol. 35, no. 8, pp. 87-105, 2008.
17. H. M. Grandin, A. C. Gemperli, and M. Dard, "Enamel matrix derivative: a review of cellular effects in vitro and a model of molecular arrangement and functioning, " Tissue Engineering B: Reviews, vol. 18, no. 3, pp. 181-202, 2012.
18. D. L. Johnson, D. Carnes, B. Steffensen, and D. L. Cochran, "Cellular effects of enamel matrix derivative are associated with different molecular weight fractions following separation by size-exclusion chomatography, " Journal of Periodontology, vol. 80, no. 4, pp. 648-656, 2009.
19. S. Suzuki, T. Nagano, Y. Yamakoshi, et al., "Enamel matrix derivative gel stimulates signal transduction of BMP and TGF-β, " Journal of Dental Research, vol. 84, no. 6, pp. 510-514, 2005.
20. K. Okubo, M. Kobayashi, T. Takiguchi, et al., "Participation of endogenous IGF-I and TGF-β1 with enamel matrix derivativestimulated cell growth in human periodontal ligament cells, " Journal of Periodontal Research, vol. 38, no. 1, pp. 1-9, 2003.
21. S. S. Prime, M. Pring, M. Davies, and I. C. Paterson, "TGF-signal transduction in oro-facial health and non-malignant disease (part I), " Critical Reviews in Oral Biology and Medicine, vol. 15, no. 6, pp. 324-336, 2004.
22. C. Sieber, J. Kopf, C. Hiepen, and P. Knaus, "Recent advances in BMP receptor signaling, " Cytokine and Growth Factor Reviews, vol. 20, no. 5-6, pp. 343-355, 2009.
23. J. Deschner and M. Nokhbehsaim, "Regulatory effects of inflammatory and biomechanical signals on regenerative periodontal healing, " International Journal of Oral & Maxillofacial Implants, vol. 28, no. 6, pp. e472-e477, 2013.
24. H. Inaba, S. Kawai, K. Nakayama, N. Okahashi, and A. Amano, "Effect of enamel matrix derivative on periodontal ligament cells in vitro is deminished by Porphyromonas gingivalis, " Journal of Periodontology, vol. 75, no. 6, pp. 858-865, 2004.
25. H. Inaba, M. Tagashira, T. Kanda, T. Ohno, S. Kawai, and A. Amano, "Apple-and hop-polyphenols protect periodontal ligament cells stimulated with enamel matrix derivative from Porphyromonas gingivalis, " Journal of Periodontology, vol. 76, no. 12, pp. 2223-2229, 2005.
26. J. Suvan, A. Petrie, D. R. Moles, et al., "Body mass index as a predictive factor of periodontal therapy outcomes, " Journal of Dental Research, vol. 93, pp. 49-54, 2014.
27. D. Lakkis, N. F. Bissada, A. Saber, et al., "Response toperiodontal therapy in patients who had weight loss after bariatric surgery and obese counterparts: a pilot study, " Journal of Periodontology, vol. 83, no. 6, pp. 684-689, 2012.
28. T. Tervonen and K. Karjalainen, "Periodontal disease related to diabetic status. A pilot study of the response to periodontal therapy in type 1 diabetes, " Journal of Clinical Periodontology, vol. 24, no. 7, pp. 505-510, 1997.
29. M. Adamczak and A. Wiecek, "The adipose tissue as an endocrine organ, " Seminars in Nephrology, vol. 33, no. 1, pp. 2-13, 2013.
30. R. Krysiak, G. Handzlik-Orlik, and B. Okopien, "The role of adipokines in connective tissue diseases, " European Journal of Nutrition, vol. 51, no. 5, pp. 513-528, 2012.
31. R. Raucci, F. Rusolo, A. Sharma, G. Colonna, G. Castello, and S. Costantini, "Functional and structural features of adipokine family, " Cytokine, vol. 61, no. 1, pp. 1-14, 2013.
32. J. van de Voorde, B. Pauwels, C. Boydens, and K. Decaluw, "Adipocytokines in relation to cardiovascular disease, " Metabolism: Clinical and Experimental, vol. 62, pp. 1513-1521, 2013.
33. K. K. Y. Cheng, K. S. L. Lam, B. Wang, and A. Xu, "Signaling mechanisms underlying the insulin-sensitizing effects of adiponectin, " Best Practice & Research Clinical Endocrinology & Metabolism, vol. 28, no. 1, pp. 3-13, 2014.
34. M. Liu and F. Liu, "Regulation of adiponectin multimerization, signaling and function, " Best Practice & Research Clinical Endocrinology & Metabolism, vol. 28, no. 1, pp. 25-31, 2014.
35. T. Yamauchi, M. Iwabu, M. Okada-Iwabu, and T. Kadowaki, "Adiponectin receptors: a reviewof their structure, function and how they work, " Best Practice Research Clinical Endocrinology& Metabolism, vol. 28, pp. 15-23, 2014.
36. F. Carbone, C. la Rocca, and G. Matarese, "Immunological functions of leptin and adiponectin, " Biochimie, vol. 94, no. 10, pp. 2082-2088, 2012.
37. G. Fantuzzi, "Adiponectin in inflammatory and immunemediated diseases, " Cytokine, vol. 64, no. 1, pp. 1-10, 2013.
38. A. T. Turer and P. E. Scherer, "Adiponectin: mechanistic insights and clinical implications, " Diabetologia, vol. 55, no. 9, pp. 2319-2326, 2012.
39. M. T. Villarreal-Molina and B. Antuna-Puente, "Adiponectin: Anti-inflammatory and cardioprotective effects, " Biochimie, vol. 94, no. 10, pp. 2143-2149, 2012.
40. D. Kraus, J. Winter, S. Jepsen, A. Jager, R. Meyer, and J. Deschner, "Interactions of adiponectin and lipopolysaccharide from Porphyromonas gingivalis on human oral epithelial cells, " PLoS ONE, vol. 7, no. 2, Article ID e30716, 2012.
41. T. Fiaschi, F. Magherini, T. Gamberi, P. A. Modesti, and A. Modesti, "Adiponectin as a tissue regenerating hormone: more than ametabolic function, " Cellular andMolecular Life Sciences, vol. 71, no. 10, pp. 1917-1925, 2014.
42. X. Chen, J. Lu, J. Bao, J. Guo, J. Shi, and Y. Wang, "Adiponectin: a biomarker for rheumatoid arthritis?" Cytokine&Growth Factor Reviews, vol. 24, no. 1, pp. 83-89, 2013.
43. M. Nokhbehsaim, J. Winter, B. Rath, A. Jager, S. Jepsen, and J. Deschner, "Effects of enamel matrix derivative on periodontal wound healing in an inflammatory environment in vitro, " Journal of Clinical Periodontology, vol. 38, no. 5, pp. 479-490, 2011.
44. M. Nokhbehsaim, B. Deschner, C. Bourauel, et al., "Interactions of enamel matrix derivative and biomechanical loading in periodontal regenerative healing, " Journal of Periodontology, vol. 82, no. 12, pp. 1725-1734, 2011.
45. M. Nokhbehsaim, S. Keser, A. Jager, et al., "Regulation of regenerative periodontal healing by NAMPT, " Mediators of Inflammation, vol. 2013, Article ID 202530, 11 pages, 2013.
46. M. Nokhbehsaim, S. Keser, A. V. B. Nogueira, et al., "Effects of Leptin on the regenerative capacity of periodontal cells, " International Journal of Endocrinology. In press.
47. G. S. Zimmermann, M. F. Bastos, T. E. D. Goncxalves, L. Chambrone, and P. M. Duarte, "Local and circulating levels of adipocytokines in obese and normal weight individuals with chronic periodontitis, " Journal of Periodontology, vol. 84, no. 5, pp. 624-633, 2013.
48. A. Damanaki, M. Nokhbehsaim, S. Eick, et al., "Regulation of NAMPT in human gingival fibroblasts and biopsies, " Mediators of Inflammation, vol. 2014, Article ID 912821, 10 pages, 2014.
49. A. V. B. Nogueira, M. Nokhbehsaim, S. Eick, et al., "Regulation of visfatin by microbial and biomechanical signals in PDL cells, " Clinical Oral Investigations, vol. 18, no. 1, pp. 171-178, 2013.
50. M. Nokhbehsaim, S. Eick, A. V. B. Nogueira, et al., "Stimulation of MMP-1 and CCL2 by NAMPT in PDL cells, " Mediators of Inflammation, vol. 2013, Article ID 437123, 12 pages, 2013.
51. Y. Arita, S. Kihara, N. Ouchi, et al., "Paradoxical decrease of an adipose-specific protein, adiponectin, in obesity, " Biochemical and Biophysical Research Communications, vol. 257, no. 1, pp. 79-83, 1999.
52. M. Cnop, P. J. Havel, K. M. Utzschneider, et al., "Relationship of adiponectin to body fat distribution, insulin sensitivity and plasma lipoproteins: evidence for independent roles of age and sex, " Diabetologia, vol. 46, no. 4, pp. 459-469, 2003.
53. C. Weyer, T. Funahashi, S. Tanaka, et al., "Hypoadiponectinemia in obesity and type 2 diabetes: close association with insulin resistance and hyperinsulinemia, " Journal of Clinical Endocrinology and Metabolism, vol. 86, no. 5, pp. 1930-1935, 2001.
54. K. Hotta, T. Funahashi, Y. Arita, et al., "Plasma concentrations of a novel, adipose-specific protein, adiponectin, in type 2 diabetic patients, " Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 20, no. 6, pp. 1595-1599, 2000.
55. A. M. Byrne, D. J. Bouchier-Hayes, and J. H. Harmey, "Angiogenic and cell survival functions of vascular endothelial growth factor (VEGF), " Journal of Cellular andMolecularMedicine, vol. 9, no. 4, pp. 777-794, 2005.
56. M. M. L. Deckers, M. Karperien, C. van der Bent, T. Yamashita, S. E. Papapoulos, and C. W. G. M. Lowik, "Expression of vascular endothelial growth factors and their receptors during osteoblast differentiation, " Endocrinology, vol. 141, no. 5, pp. 1667-1674, 2000.
57. N. Ferrara, "Role of vascular endothelial growth factor in the regulation of angiogenesis, " Kidney International, vol. 56, no. 3, pp. 794-814, 1999.
58. Y. Seomun, J.-T. Kim, and C.-K. Joo, "MMP-14 mediated MMP-9 expression is involved in TGF-beta1-induced keratinocyte migration, " Journal of Cellular Biochemistry, vol. 104, no. 3, pp. 934-941, 2008.
59. P. Sysa, J. J. Potter, X. Liu, and E. Mezey, "Transforming growth factor-β1 up-regulation of human 1(I) collagen is mediated by Sp1 and Smad2 transacting factors, " DNA and Cell Biology, vol. 28, no. 9, pp. 425-434, 2009.
60. M. Valluru, C. A. Staton, M. W. R. Reed, and N. J. Brown, "Transforming growth factor-and endoglin signaling orchestrate wound healing, " Frontiers in Physiology, vol. 2, article 89, 2011.
61. D. W. Hamilton, "Functional role of periostin in development and wound repair: implications for connective tissue disease, " Journal of Cell Communication and Signaling, vol. 2, no. 1-2, pp. 9-17, 2008.
62. H. F. Rios, D. Ma, Y. Xie, et al., "Periostin is essential for the integrity and function of the periodontal ligament during occlusal loading in mice, " Journal of Periodontology, vol. 79, no. 8, pp. 1480-1490, 2008.
63. G. E. Romanos, K. P. Asnani, D. Hingorani, and V. L. Deshmukh, "PERIOSTIN: role in formation and maintenance of dental tissues, " Journal of Cellular Physiology, vol. 229, no. 1, pp. 1-5, 2014.
64. P. J. Marie, "Transcription factors controlling osteoblastogenesis, " Archives of Biochemistry and Biophysics, vol. 473, no. 2, pp. 98-105, 2008.
65. T. Iwayama, M. Yanagita, K. Mori, et al., "Adiponectin regulates functions of gingival fibroblasts and periodontal ligament cells, " Journal of Periodontal Research, vol. 47, no. 5, pp. 563-571, 2012.
66. Y. Yasuda, T. Koike, T. Kawamorita, and T. Saito, "Adiponectin induces dentin sialophosphoprotein in rat dental pulp cells: an in vitro study, " Journal of Endodontics, vol. 34, no. 6, pp. 679-683, 2008.
67. N. Yamaguchi, T. Kukita, Y. Li, et al., "Adiponectin inhibits induction of TNF-/RANKL-stimulatedNFATc1 via theAMPK signaling, "The FEBS Letters, vol. 582, no. 3, pp. 451-456, 2008.
68. Q. Tu, J. Zhang, L. Q. Dong, et al., "Adiponectin inhibits osteoclastogenesis and bone resorption via APPL1-mediated suppression of Akt1, " Journal of Biological Chemistry, vol. 286, no. 14, pp. 12542-12553, 2011.
69. E. Luo, J. Hu, C. Bao, et al., "Sustained release of adiponectin improves osteogenesis around hydroxyapatite implants by suppressing osteoclast activity in ovariectomized rabbits, " Acta Biomaterialia, vol. 8, no. 2, pp. 734-743, 2012.
70. N. Kamio, S. Akifusa, N. Yamaguchi, K. Nonaka, and Y. Yamashita, "Anti-inflammatory activity of a globular adiponectin function on RAW 264 cells stimulated by lipopolysaccharide from Aggregatibacter actinomycetemcomitans, " FEMS Immunology and Medical Microbiology, vol. 56, no. 3, pp. 241-247, 2009.
71. K. Zhang, X. Zhang, L. Y. Yu, and B. Y. Xu, "The effect of adiponectin on human periodontal ligament fibroblasts in vitro, " Shanghai Kou Qiang Yi Xue, vol. 21, pp. 48-52, 2012.
72. H. G. Park, E. J. Bak, J. H. Kim, et al., "Effect of globular adiponectin on interleukin-6 and interleukin-8 expression in periodontal ligament and gingival fibroblasts, " Journal of Periodontal and Implant Science, vol. 41, no. 3, pp. 149-156, 2011.
73. L. Kardeser, N. Buduneli, S Cetinkalp, and D. F. Kinane, "Adipokines and inflammatory mediators after initial periodontal treatment in patients with type 2 diabetes and chronic periodontitis, " Journal of Periodontology, vol. 81, no. 1, pp. 24-33, 2010.
74. P. Bharti, S. Katagiri, H. Nitta, et al., "Periodontal treatmentwith topical antibiotics improves glycemic control in association with elevated serumadiponectin in patients with type 2 diabetes mellitus, " Obesity Research and Clinical Practice, vol. 7, no. 2, pp. e129-e138, 2013.
75. W.-L. Sun, L.-L. Chen, S.-Z. Zhang, Y.-W. Wu, Y.-Z. Ren, and G.-M. Qin, "Infammatory cytokines, adiponectin, insulin resistance and metabolic control after periodontal intervention in patients with type 2 diabetes and chronic periodontitis, " Internal Medicine, vol. 50, no. 15, pp. 1569-1574, 2011.
76. J. Honig, C. Rordorf-Adam, C. Siegmund, W. Wiedemann, and F. Erard, "Increased interleukin-1-beta (IL-1β) concentration in gingival tissue fromperiodontitis patients, " Journal of Periodontal Research, vol. 24, no. 6, pp. 362-367, 1989.
77. L. T. Hou, C. M. Liu, and W. K. Chang, "Increased interleukin-1 beta levels in gingival crevicular fluid of Chinese periodontal patients., " Journal of the FormosanMedical Association, vol. 93, no. 2, pp. 99-103, 1994.
78. A. Mathur, B. Michalowicz, M. Castillo, and D. Aeppli, "Interleukin-1 alpha, interleukin-8 and interferon-alpha levels in gingival crevicular fluid, " Journal of Periodontal Research, vol. 31, no. 7, pp. 489-495, 1996.
79. S. C. Holt and J. L. Ebersole, "Porphyromonas gingivalis, Treponema denticola, and Tannerella forsythia: the red complex, a prototype polybacterial pathogenic consortium in periodontitis, " Periodontology 2000, vol. 38, pp. 72-122, 2005.
80. K. Nakayama, "Molecular genetics of Porphyromonas gingivalis: gingipains and other virulence factors, " Current Protein and Peptide Science, vol. 4, no. 6, pp. 389-395, 2003.
81. J. Potempa, A. Sroka, T. Imamura, and J. Travis, "Gingipains, the major cysteine proteinases and virulence factors of Porphyromonas gingivalis: structure, function and assembly of multidomain protein complexes, " Current Protein and Peptide Science, vol. 4, no. 6, pp. 397-407, 2003.
82. Y. W. Han, W. Shi, G. T. Huang, et al., "Interactions between periodontal bacteria and human oral epithelial cells: Fusobacterium nucleatum adheres to and invades epithelial cells, " Infection and Immunity, vol. 68, no. 6, pp. 3140-3146, 2000.
83. J. He, W. Huang, Z. Pan, et al., "Quantitative analysis of microbiota in saliva, supragingival, and subgingival plaque of Chinese adults with chronic periodontitis, " Clinical Oral Investigations, vol. 16, no. 6, pp. 1579-1588, 2012.
84. B. Signat, C. Roques, P. Poulet, and D. Duffaut, "Fusobacterium nucleatum in periodontal health and disease, " Current Issues in Molecular Biology, vol. 13, no. 2, pp. 25-36, 2011.