Evaluation of the effect of oleuropein on alveolar bone loss, inflammation, and apoptosis in experimental periodontitis.
Alveolar Bone Loss
/ drug therapy
Animals
Antigens, CD
/ metabolism
Antigens, Differentiation, Myelomonocytic
/ metabolism
Apoptosis
Bone Morphogenetic Protein 4
/ metabolism
Caspase 3
/ metabolism
Female
Inflammation
/ drug therapy
Iridoid Glucosides
Iridoids
/ pharmacology
Nitric Oxide Synthase Type II
/ metabolism
Osteoblasts
/ cytology
Osteoclasts
/ cytology
Periodontitis
/ drug therapy
Proto-Oncogene Proteins c-bcl-2
/ metabolism
Rats
Rats, Wistar
Tartrate-Resistant Acid Phosphatase
/ metabolism
BMP-4
CD-68
TRAP
alveolar bone
experimental periodontitis
oleuropein
Journal
Journal of periodontal research
ISSN: 1600-0765
Titre abrégé: J Periodontal Res
Pays: United States
ID NLM: 0055107
Informations de publication
Date de publication:
Dec 2019
Dec 2019
Historique:
received:
14
11
2018
revised:
19
03
2019
accepted:
30
03
2019
pubmed:
30
4
2019
medline:
16
1
2020
entrez:
30
4
2019
Statut:
ppublish
Résumé
The present study aimed to evaluate the effects of oleuropein on ligature-induced alveolar bone loss. In this respect, osteoblastic activity, osteoclastic activity, inflammatory markers, and apoptosis were evaluated. Oleuropein is a flavonoid, which has potent anti-inflammatory and bone-protective effects. Thirty-two Wistar rats were divided into four experimental groups as following: control (C, n = 8) group; periodontitis (P, n = 8) group; periodontitis and low-dose oleuropein group (12 mg/kg/day oleuropein, LDO group, n = 8); and periodontitis and high-dose oleuropein group (24 mg/kg/day oleuropein, HDO group, n = 8). Periodontitis was induced via ligatures. Study period was 14 days, and animals were sacrificed at end of this period. Mandibles were examined via a stereomicroscope and underwent histological procedures. Osteoblast, tartrate-resistant acid phosphatase (TRAP)-positive osteoclast, and inflammatory cell counts were determined in hematoxylin-eosin stained sections. Inducible nitric oxide synthase (iNOS), bone morphogenetic protein-4, the cluster of differentiation (CD)-68, cysteine-aspartic proteases-3 (Caspase 3), and B-cell lymphoma-2 (Bcl-2) expressions were evaluated via immunohistochemistry. Periodontitis group had highest alveolar bone loss, and these levels significantly decreased in LDO and HDO groups. Both 12 and 24 mg/kg oleuropein groups significantly increased osteoblast cell counts and decreased TRAP-positive osteoclast and inflammatory cell counts. BMP-4 and bcl-2 expressions were elevated in oleuropein groups while caspase-3 expressions decreased. iNOS and CD68 were higher in periodontitis group compared to control group, but there was no significant difference between other groups. Oleuropein successfully decreased alveolar bone loss as a result of decreased osteoclastic activity, inflammation, and apoptosis and increased osteoblastic activity.
Sections du résumé
THE OBJECTIVE
OBJECTIVE
The present study aimed to evaluate the effects of oleuropein on ligature-induced alveolar bone loss. In this respect, osteoblastic activity, osteoclastic activity, inflammatory markers, and apoptosis were evaluated.
BACKGROUND
BACKGROUND
Oleuropein is a flavonoid, which has potent anti-inflammatory and bone-protective effects.
METHODS
METHODS
Thirty-two Wistar rats were divided into four experimental groups as following: control (C, n = 8) group; periodontitis (P, n = 8) group; periodontitis and low-dose oleuropein group (12 mg/kg/day oleuropein, LDO group, n = 8); and periodontitis and high-dose oleuropein group (24 mg/kg/day oleuropein, HDO group, n = 8). Periodontitis was induced via ligatures. Study period was 14 days, and animals were sacrificed at end of this period. Mandibles were examined via a stereomicroscope and underwent histological procedures. Osteoblast, tartrate-resistant acid phosphatase (TRAP)-positive osteoclast, and inflammatory cell counts were determined in hematoxylin-eosin stained sections. Inducible nitric oxide synthase (iNOS), bone morphogenetic protein-4, the cluster of differentiation (CD)-68, cysteine-aspartic proteases-3 (Caspase 3), and B-cell lymphoma-2 (Bcl-2) expressions were evaluated via immunohistochemistry.
RESULTS
RESULTS
Periodontitis group had highest alveolar bone loss, and these levels significantly decreased in LDO and HDO groups. Both 12 and 24 mg/kg oleuropein groups significantly increased osteoblast cell counts and decreased TRAP-positive osteoclast and inflammatory cell counts. BMP-4 and bcl-2 expressions were elevated in oleuropein groups while caspase-3 expressions decreased. iNOS and CD68 were higher in periodontitis group compared to control group, but there was no significant difference between other groups.
CONCLUSION
CONCLUSIONS
Oleuropein successfully decreased alveolar bone loss as a result of decreased osteoclastic activity, inflammation, and apoptosis and increased osteoblastic activity.
Substances chimiques
Antigens, CD
0
Antigens, Differentiation, Myelomonocytic
0
Bcl2 protein, rat
0
Bmp4 protein, rat
0
Bone Morphogenetic Protein 4
0
CD68 protein, rat
0
Iridoid Glucosides
0
Iridoids
0
Proto-Oncogene Proteins c-bcl-2
0
oleuropein
2O4553545L
Nitric Oxide Synthase Type II
EC 1.14.13.39
Nos2 protein, rat
EC 1.14.13.39
Tartrate-Resistant Acid Phosphatase
EC 3.1.3.2
Casp3 protein, rat
EC 3.4.22.-
Caspase 3
EC 3.4.22.-
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
624-632Informations de copyright
© 2019 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd.
Références
Listgarten MA. Nature of periodontal diseases: pathogenic mechanisms. J Periodontal Res. 1987;22:172-178.
Haffajee AD, Socransky SS. Microbial etiological agents of destructive periodontal diseases. Periodontol 2000. 1994;5:78-111.
Pihlstrom BL, Michalowicz BS, Johnson NW. Periodontal diseases. Lancet. 2005;366:1809-1820.
Ebersole JL, Taubman MA. The protective nature of host responses in periodontal diseases. Periodontol 2000. 1994;5:112-141.
Offenbacher S. Periodontal diseases: pathogenesis. Ann Periodontol. 1996;1:821-878.
Cekici A, Kantarci A, Hasturk H, Van Dyke TE. Inflammatory and immune pathways in the pathogenesis of periodontal disease. Periodontol 2000. 2014;64:57-80.
Freire MO, Van Dyke TE. Natural resolution of inflammation. Periodontol 2000. 2013;63:149-164.
Serhan CN, Brain SD, Buckley CD, et al. Resolution of inflammation: state of the art, definitions and terms. FASEB J. 2007;21:325-332.
Faienza MF, Ventura A, Marzano F, Cavallo L. Postmenopausal osteoporosis: the role of immune system cells. Clin Dev Immunol. 2013;2013:575936.
Komatsu N, Takayanagi H. Immune-bone interplay in the structural damage in rheumatoid arthritis. Clin Exp Immunol. 2018;194:1-8.
Poligone B, Baldwin AS. Positive and negative regulation of NF-kappaB by COX-2: roles of different prostaglandins. J Biol Chem. 2001;274:38658-38664.
Dar HY, Azam Z, Anupam R, Mondal RK, Srivastava RK. Osteoimmunology: the Nexus between bone and immune system. Front Biosci. 2018;23:464-492.
Song J, Jing Z, Hu W, Yu J, Cui X. α-Linolenic acid inhibits receptor activator of NF-κB ligand induced (RANKL-induced) osteoclastogenesis and prevents inflammatory bone loss via downregulation of nuclear Factor-KappaB-inducible nitric oxide synthases (NF-κB-iNOS) signaling pathways. Med Sci Monit. 2017;23:5056.
Manthiram K, Zhou Q, Aksentijevich I, Kastner DL. The monogenic autoinflammatory diseases define new pathways in human innate immunity and inflammation. Nat Immunol. 2017;18:832.
Livolsi A, Busuttil V, Imbert V, Abraham RT, Peyron JF. Tyrosine phosphorylation-dependent activation of NF-κB: requirement for p56 LCK and ZAP-70 protein tyrosine kinases. Eur J Biochem. 2001;268:1508-1515.
Gupta SC, Kunnumakkara AB, Aggarwal S, Aggarwal BB. Inflammation, a double-edge sword for cancer and other age-related diseases. Front Immunol. 2018;9:2160.
Korbecki J, Baranowska-Bosiacka I, Gutowska I, Chlubek D. The effect of reactive oxygen species on the synthesis of prostanoids from arachidonic acid. J Physiol Pharmacol. 2013;64:409-421.
Scoditti E, Calabriso N, Massaro M, et al. Mediterranean diet polyphenols reduce inflammatory angiogenesis through MMP-9 and COX-2 inhibition in human vascular endothelial cells: a potentially protective mechanism in atherosclerotic vascular disease and cancer. Arch Biochem Biophys. 2012;527:81-89.
Scoditti E, Nestola A, Massaro M, et al. Hydroxytyrosol suppresses MMP-9 and COX-2 activity and expression in activated human monocytes via PKCα and PKCβ1 inhibition. Atherosclerosis. 2014;232:17-24.
Wang L, Geng C, Jiang L, et al. The anti-atherosclerotic effect of olive leaf extract is related to suppressed inflammatory response in rabbits with experimental atherosclerosis. Eur J Nutr. 2008;47:235-243.
Andreadou I, Mikros E, Ioannidis K, et al. Oleuropein prevents doxorubicin-induced cardiomyopathy interfering with signaling molecules and cardiomyocyte metabolism. J Mol Cell Cardiol. 2014;69:4-16.
Bendini A, Cerretani L, Carrasco-Pancorbo A, et al. Phenolic molecules in virgin olive oils: a survey of their sensory properties, health effects, antioxidant activity and analytical methods. An overview of the last decade Alessandra. Molecules 2007;12:1679-1719.
Puel C, Quintin A, Agalias A, et al. Olive oil and its main phenolic micronutrient (oleuropein) prevent inflammation-induced bone loss in the ovariectomised rat. Br J Nutr. 2004;92:119-127.
Puel C, Mathey J, Agalias A, et al. Dose-response study of effect of oleuropein, an olive oil polyphenol, in an ovariectomy/inflammation experimental model of bone loss in the rat. Clin Nutr. 2006;25:859-868.
Hagiwara K, Goto T, Araki M, Miyazaki H, Hagiwara H. Olive polyphenol hydroxytyrosol prevents bone loss. Eur J Pharmacol. 2011;662:78-84.
Santiago-Mora R, Casado-Diaz A, De Castro M, Quesada-Gomez J. Oleuropein enhances osteoblastogenesis and inhibits adipogenesis: the effect on differentiation in stem cells derived from bone marrow. Osteoporos Int. 2011;22:675-684.
García-Martínez O, Mazzaglia G, Sánchez-Ortiz A, Ocaña-Peinado FM, Rivas A. Phenolic content of Sicilian virgin olive oils and their effect on MG-63 human osteoblastic cell proliferation. Grasas Aceites 2014;65:e032.
Häkkinen L, Larjava H, Fournier BP. Distinct phenotype and therapeutic potential of gingival fibroblasts. Cytotherapy. 2014;16:1171-1186.
Fournier BP, Larjava H, Häkkinen L. Gingiva as a source of stem cells with therapeutic potential. Stem Cells Dev. 2013;22:3157-3177.
Balci Yuce H, Akbulut N, Ocakli S, Kayir O, Elmastas M. The effect of commercial conjugated linoleic acid products on experimental periodontitis and diabetes mellitus in Wistar rats. Acta Odontol Scand. 2017;75:21-29.
Balci Yuce H, Karatas Ö, Tulu F, Altan A, Gevrek F. Effect of diabetes on collagen metabolism and hypoxia in human gingival tissue: a stereological, histopathological, and immunohistochemical study. Biotech Histochem. 2018;94:1-9.
Toker H, Balci Yuce H, Lektemur Alpan A, Gevrek F, Elmastas M. Morphometric and histopathological evaluation of the effect of grape seed proanthocyanidin on alveolar bone loss in experimental diabetes and periodontitis. J Periodontal Res. 2018;53:478-486.
Xing T, Wang Y, Ding W-J, et al. Thrombospondin-1 production regulates the inflammatory cytokine secretion in THP-1 cells through NF-κB signaling pathway. Inflammation 2017;40:1606-1621.
Balci Yuce H, Lektemur Alpan A, Gevrek F, Toker H. Investigation of the effect of astaxanthin on alveolar bone loss in experimental periodontitis. J Periodontal Res. 2018;53:131-138.
Fan H, Hui J, Duan Z, et al. Novel scaffolds fabricated using oleuropein for bone tissue engineering. Biomed Res Int. 2014;2014:652432.
Filip R, Possemiers S, Heyerick A, et al. Twelve-month consumption of a polyphenol extract from olive (Olea europaea) in a double blind, randomized trial increases serum total osteocalcin levels and improves serum lipid profiles in postmenopausal women with osteopenia. J Nutr Health Aging. 2015;19:77-86.
García-Martínez O, De Luna-Bertos E, Ramos-Torrecillas J, et al. Phenolic compounds in extra virgin olive oil stimulate human osteoblastic cell proliferation. PLoS ONE. 2016;11:e0150045.
Wang Y, He H, Cao Z, Fang Y, Du M, Liu Z. Regulatory effects of bone morphogenetic protein-4 on tumour necrosis factor-α-suppressed Runx2 and osteoprotegerin expression in cementoblasts. Cell Prolif. 2017;50:e12344.
Fujita K, Otsuka T, Yamamoto N, et al. (-)-Epigallocatechin gallate but not chlorogenic acid upregulates osteoprotegerin synthesis through regulation of bone morphogenetic protein-4 in osteoblasts. Exp Ther Med. 2017;14:417-423.
Kim Y-H, Choi Y-J, Kang M-K, et al. Oleuropein curtails pulmonary inflammation and tissue destruction in models of experimental asthma and emphysema. J Agric Food Chem. 2018;66:7643-7654.
Jayaprakash K, Demirel I, Gunaltay S, Khalaf H, Bengtsson T. PKC, ERK/p38 MAP kinases and NF-κB targeted signalling play a role in the expression and release of IL-1β and CXCL8 in Porphyromonas gingivalis-infected THP1 cells. APMIS. 2017;125:623-633.
Woźniak M, Michalak B, Wyszomierska J, Dudek MK, Kiss AK. Effects of phytochemically characterized extracts from syringa vulgaris and isolated secoiridoids on mediators of inflammation in a human neutrophil model. Front Pharmacol. 2018;9:349.
Castejón ML, Rosillo MÁ, Montoya T, González-Benjumea A, Fernández-Bolaños JM, Alarcón-de-la-Lastra C. Oleuropein down-regulated IL-1β-induced inflammation and oxidative stress in human synovial fibroblast cell line SW982. Food Funct. 2017;8:1890-1898.
Feng Z, Li X, Lin J, et al. Oleuropein inhibits the IL-1β-induced expression of inflammatory mediators by suppressing the activation of NF-κB and MAPKs in human osteoarthritis chondrocytes. Food Funct. 2017;8:3737-3744.
Alves AM, Diel LF, Lamers ML. Macrophages and prognosis of oral squamous cell carcinoma: a systematic review. J Oral Pathol Med. 2018;47:460-467.
Xue L, Su L, Zhao L, Li J, Du Y, Yu X. Cyclophilin a increases CD68 + cell infiltration in rat experimental periodontitis. J Mol Histol. 2018;49:157-164.
Zhang W, Liu X, Li Q. Protective effects of oleuropein against cerebral ischemia/reperfusion by inhibiting neuronal apoptosis. Med Sci Monit. 2018;24:6587.
Potočnjak I, Škoda M, Pernjak-Pugel E, Peršić MP, Domitrović R. Oral administration of oleuropein attenuates cisplatin-induced acute renal injury in mice through inhibition of ERK signaling. Mol Nutr Food Res. 2016;60:530-541.
Koc K, Cerig S, Ozek NS, et al. The efficacy of oleuropein against non-steroidal anti-inflammatory drug induced toxicity in rat kidney. Environ Toxicol. 2018;34:67-72.
Alirezaei M, Dezfoulian O, Neamati S, Rashidipour M, Tanideh N, Kheradmand A. Oleuropein prevents ethanol-induced gastric ulcers via elevation of antioxidant enzyme activities in rats. J Physiol Biochem. 2012;68:583-592.