Top

Published in:

01-09-2016 | Original Article

Hypoxia enhances the effect of lipopolysaccharide-stimulated IL-1β expression in human periodontal ligament cells

Authors: Jittima Pumklin, Kanokporn Bhalang, Prasit Pavasant

Published in: Odontology | Issue 3/2016

Abstract

Oral infection is inflammatory disease caused by bacteria. A major component of gram negative bacteria membrane associated with inflammation is lipopolysaccharide (LPS). Currently, evidence presenting the combined effect of LPS and hypoxia to inflammatory response in human periodontal ligament cells (HPDLs) was yet lacking. Here, we studied whether the influence of oxygen on LPS-stimulated inflammatory cytokines in HPDLs. HPDLs were stimulated with LPS in normoxia and hypoxia for 24 h. The mRNA and protein expression of inflammatory cytokines were examined by polymerase chain reaction and enzyme-linked immunosorbent assay, respectively. The intracellular mechanisms of these effects were investigated by chemical inhibitors and small interfering RNA (siRNA). The results showed that LPS-stimulated IL-1β, IL-6, IL-8 in HPDLs in both hypoxia and normoxia. Hypoxia condition enhanced the effect of LPS-stimulated cytokines expression. Apigenin, the hypoxia-inducible factors (HIF)-1α inhibitor, totally prevented LPS-stimulated IL-1β expression in both normoxia and hypoxia. Similar to knockout HIF-1α gene expression by siRNA did \not prevent LPS-stimulated IL-1β expression. These data concluded that hypoxia increased virulence of LPS-stimulated IL-1β production in HPDLs.

Akira S, Uematsu S, Takeuchi O. Pathogen recognition and innate immunity. Cell. 2006;124(4):783–801. doi:10.1016/j.cell.2006.02.015.CrossRefPubMed

Rizzo A, Bevilacqua N, Guida L, Annunziata M, Romano Carratelli C, Paolillo R. Effect of resveratrol and modulation of cytokine production on human periodontal ligament cells. Cytokine. 2012;60(1):197–204. doi:10.1016/j.cyto.2012.06.004.CrossRefPubMed

Jeong GS, Lee SH, Jeong SN, Kim YC, Kim EC. Anti-inflammatory effects of apigenin on nicotine- and lipopolysaccharide-stimulated human periodontal ligament cells via heme oxygenase-1. Int Immunopharmacol. 2009;9(12):1374–80. doi:10.1016/j.intimp.2009.08.015.CrossRefPubMed

Kim YS, Shin SI, Kang KL, Chung JH, Herr Y, Bae WJ, et al. Nicotine and lipopolysaccharide stimulate the production of MMPs and prostaglandin E2 by hypoxia-inducible factor-1alpha up-regulation in human periodontal ligament cells. J Periodontal Res. 2012;47(6):719–28. doi:10.1111/j.1600-0765.2012.01487.x.CrossRefPubMed

Yamaji Y, Kubota T, Sasaguri K, Sato S, Suzuki Y, Kumada H, et al. Inflammatory cytokine gene expression in human periodontal ligament fibroblasts stimulated with bacterial lipopolysaccharides. Infect Immun. 1995;63(9):3576–81.PubMedPubMedCentral

Seo T, Cha S, Kim TI, Lee JS, Woo KM. Porphyromonas gingivalis-derived lipopolysaccharide-mediated activation of MAPK signaling regulates inflammatory response and differentiation in human periodontal ligament fibroblasts. J Microbiol. 2012;50(2):311–9. doi:10.1007/s12275-012-2146-x.CrossRefPubMed

Jian C, Li C, Ren Y, He Y, Li Y, Feng X, et al. Hypoxia augments lipopolysaccharide-induced cytokine expression in periodontal ligament cells. Inflammation. 2014;37(5):1413–23. doi:10.1007/s10753-014-9865-6.CrossRefPubMed

Finney SJ, Leaver SK, Evans TW, Burke-Gaffney A. Differences in lipopolysaccharide- and lipoteichoic acid-induced cytokine/chemokine expression. Intensive Care Med. 2012;38(2):324–32. doi:10.1007/s00134-011-2444-5.CrossRefPubMed

Seehase S, Lauenstein HD, Schlumbohm C, Switalla S, Neuhaus V, Forster C, et al. LPS-induced lung inflammation in marmoset monkeys—an acute model for anti-inflammatory drug testing. PLoS One. 2012;7(8):e43709. doi:10.1371/journal.pone.0043709.CrossRefPubMedPubMedCentral

10.

Takeda K, Akira S. TLR signaling pathways. Semin Immunol. 2004;16(1):3–9. doi:10.1016/j.smim.2003.10.003.CrossRefPubMed

11.

Safronova O, Morita I. Transcriptome remodeling in hypoxic inflammation. J Dent Res. 2010;89(5):430–44. doi:10.1177/0022034510366813.CrossRefPubMed

12.

Chang N, Goodson WH 3rd, Gottrup F, Hunt TK. Direct measurement of wound and tissue oxygen tension in postoperative patients. Ann Surg. 1983;197(4):470–8.CrossRefPubMedPubMedCentral

13.

Karhausen J, Haase VH, Colgan SP. Inflammatory hypoxia: role of hypoxia-inducible factor. Cell cycle (Georgetown, Tex). 2005;4(2):256–8.

14.

Eltzschig HK, Carmeliet P. Hypoxia and inflammation. N Engl J Med. 2011;364(7):656–65. doi:10.1056/NEJMra0910283.CrossRefPubMedPubMedCentral

15.

Brahimi-Horn MC, Pouyssegur J. Oxygen, a source of life and stress. FEBS Lett. 2007;581(19):3582–91. doi:10.1016/j.febslet.2007.06.018.CrossRefPubMed

16.

Ke Q, Costa M. Hypoxia-inducible factor-1 (HIF-1). Mol Pharmacol. 2006;70(5):1469–80. doi:10.1124/mol.106.027029.CrossRefPubMed

17.

Hempel SL, Monick MM, Hunninghake GW. Effect of hypoxia on release of IL-1 and TNF by human alveolar macrophages. Am J Respir Cell Mol Biol. 1996;14(2):170–6. doi:10.1165/ajrcmb.14.2.8630267.CrossRefPubMed

18.

Jeong HJ, Hong SH, Park RK, Shin T, An NH, Kim HM. Hypoxia-induced IL-6 production is associated with activation of MAP kinase, HIF-1, and NF-kappaB on HEI-OC1 cells. Hear Res. 2005;207(1–2):59–67. doi:10.1016/j.heares.2005.04.003.CrossRefPubMed

19.

Chandel NS, Trzyna WC, McClintock DS, Schumacker PT. Role of oxidants in NF-kappa B activation and TNF-alpha gene transcription induced by hypoxia and endotoxin. J Immunol. 2000;165(2):1013–21.CrossRefPubMed

20.

Jian C, Li C, Ren Y, He Y, Li Y, Feng X, et al. Hypoxia augments lipopolysaccharide-induced cytokine expression in periodontal ligament cells. Inflammation. 2014;. doi:10.1007/s10753-014-9865-6.PubMed

21.

Kim SY, Choi YJ, Joung SM, Lee BH, Jung YS, Lee JY. Hypoxic stress up-regulates the expression of Toll-like receptor 4 in macrophages via hypoxia-inducible factor. Immunology. 2010;129(4):516–24. doi:10.1111/j.1365-2567.2009.03203.x.CrossRefPubMedPubMedCentral

22.

Dinarello CA. Interleukin-1 in the pathogenesis and treatment of inflammatory diseases. Blood. 2011;117(14):3720–32. doi:10.1182/blood-2010-07-273417.CrossRefPubMedPubMedCentral

23.

Boch JA, Wara-aswapati N, Auron PE. Interleukin 1 signal transduction—current concepts and relevance to periodontitis. J Dent Res. 2001;80(2):400–7.CrossRefPubMed

24.

Fang J, Xia C, Cao Z, Zheng JZ, Reed E, Jiang BH. Apigenin inhibits VEGF and HIF-1 expression via PI3 K/AKT/p70S6K1 and HDM2/p53 pathways. FASEB J. 2005;19(3):342–53. doi:10.1096/fj.04-2175com.CrossRefPubMed

25.

Ye J, Gao Z, Yin J, He Q. Hypoxia is a potential risk factor for chronic inflammation and adiponectin reduction in adipose tissue of ob/ob and dietary obese mice. Am J Physiol Endocrinol Metab. 2007;293(4):E1118–28. doi:10.1152/ajpendo.00435.2007.CrossRefPubMed

26.

Ndengele MM, Bellone CJ, Lechner AJ, Matuschak GM. Brief hypoxia differentially regulates LPS-induced IL-1beta and TNF-alpha gene transcription in RAW 264.7 cells. Am J Physiol Lung Cell Mol Physiol 2000;278(6):L1289–96.

27.

Nizet V, Johnson RS. Interdependence of hypoxic and innate immune responses. Nat Rev Immunol. 2009;9(9):609–17. doi:10.1038/nri2607.CrossRefPubMedPubMedCentral

28.

Bowie A, O’Neill LA. The interleukin-1 receptor/Toll-like receptor superfamily: signal generators for pro-inflammatory interleukins and microbial products. J Leukoc Biol. 2000;67(4):508–14.PubMed

29.

Nukaga J, Kobayashi M, Shinki T, Song H, Takada T, Takiguchi T, et al. Regulatory effects of interleukin-1beta and prostaglandin E2 on expression of receptor activator of nuclear factor-kappaB ligand in human periodontal ligament cells. J Periodontol. 2004;75(2):249–59. doi:10.1902/jop.2004.75.2.249.CrossRefPubMed

30.

Lee YM, Fujikado N, Manaka H, Yasuda H, Iwakura Y. IL-1 plays an important role in the bone metabolism under physiological conditions. Int Immunol. 2010;22(10):805–16. doi:10.1093/intimm/dxq431.CrossRefPubMed

31.

Wada N, Maeda H, Yoshimine Y, Akamine A. Lipopolysaccharide stimulates expression of osteoprotegerin and receptor activator of NF-kappa B ligand in periodontal ligament fibroblasts through the induction of interleukin-1 beta and tumor necrosis factor-alpha. Bone. 2004;35(3):629–35. doi:10.1016/j.bone.2004.04.023.CrossRefPubMed

32.

Motohira H, Hayashi J, Tatsumi J, Tajima M, Sakagami H, Shin K. Hypoxia and reoxygenation augment bone-resorbing factor production from human periodontal ligament cells. J Periodontol. 2007;78(9):1803–9. doi:10.1902/jop.2007.060519.CrossRefPubMed

33.

Anso E, Zuazo A, Irigoyen M, Urdaci MC, Rouzaut A, Martinez-Irujo JJ. Flavonoids inhibit hypoxia-induced vascular endothelial growth factor expression by a HIF-1 independent mechanism. Biochem Pharmacol. 2010;79(11):1600–9. doi:10.1016/j.bcp.2010.02.004.CrossRefPubMed

34.

Nicholas C, Batra S, Vargo MA, Voss OH, Gavrilin MA, Wewers MD, et al. Apigenin blocks lipopolysaccharide-induced lethality in vivo and proinflammatory cytokines expression by inactivating NF-kappaB through the suppression of p65 phosphorylation. Journal of immunology. 2007;179(10):7121–7.CrossRef

35.

Rider P, Kaplanov I, Romzova M, Bernardis L, Braiman A, Voronov E, et al. The transcription of the alarmin cytokine interleukin-1 alpha is controlled by hypoxia inducible factors 1 and 2 alpha in hypoxic cells. Front Immunol. 2012;3:290. doi:10.3389/fimmu.2012.00290.CrossRefPubMedPubMedCentral

36.

Ryu JH, Chae CS, Kwak JS, Oh H, Shin Y, Huh YH, et al. Hypoxia-inducible factor-2alpha is an essential catabolic regulator of inflammatory rheumatoid arthritis. PLoS Biol. 2014;12(6):e1001881. doi:10.1371/journal.pbio.1001881.CrossRefPubMedPubMedCentral

Title: Hypoxia enhances the effect of lipopolysaccharide-stimulated IL-1β expression in human periodontal ligament cells
Authors: Jittima Pumklin
Kanokporn Bhalang
Prasit Pavasant
Publication date: 01-09-2016
Publisher: Springer Japan
Published in: Odontology / Issue 3/2016
Print ISSN: 1618-1247
Electronic ISSN: 1618-1255
DOI: https://doi.org/10.1007/s10266-015-0223-4

At a glance: The STEP trials

Springer Medicine

Hypoxia enhances the effect of lipopolysaccharide-stimulated IL-1β expression in human periodontal ligament cells

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 3/2016

Evaluation of dental implants as a risk factor for the development of bisphosphonate-related osteonecrosis of the jaw in breast cancer patients

Prevalence and distribution of anomalies of permanent dentition in 9584 Japanese high school students

Performance of NiTi endodontic instrument under different temperatures

Polymerization shrinkage assessment of dental resin composites: a literature review

Salivary-free fluoride ion concentration measured using a flow-injection analysis device and oral environment in 4–6-year-old children

Amelogenesis imperfecta: review of diagnostic findings and treatment concepts